Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

Class I ventral posterior dendritic arborisation (c1vpda) proprioceptive sensory neurons respond to contractions in the Drosophila larval body wall during crawling. Their dendritic branches run along the direction of contraction, possibly a functional requirement to maximise membrane curvature during crawling contractions. Although the molecular machinery of dendritic patterning in c1vpda has been extensively studied, the process leading to the precise elaboration of their comb-like shapes remains elusive. Here, to link dendrite shape with its proprioceptive role, we performed long-term, non-invasive, in vivo time-lapse imaging of c1vpda embryonic and larval morphogenesis to reveal a sequence of differentiation stages. We combined computer models and dendritic branch dynamics tracking to propose that distinct sequential phases of stochastic growth and retraction achieve efficient dendritic trees both in terms of wire and function. Our study shows how dendrite growth balances structure–function requirements, shedding new light on general principles of self-organisation in functionally specialised dendrites.

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Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

10.1101/2020.07.09.195446 ◽

2020 ◽

Cited By ~ 1

Author(s):

André Ferreira Castro ◽

Lothar Baltruschat ◽

Tomke Stürner ◽

Amirhoushang Bahrami ◽

Peter Jedlicka ◽

...

Keyword(s):

Body Wall ◽

Time Lapse ◽

Membrane Curvature ◽

Class I ◽

List Type ◽

Larval Body ◽

And Function ◽

Dendritic Branches ◽

Time Lapse Imaging

AbstractClass I ventral posterior dendritic arborisation (c1vpda) proprioceptive sensory neurons respond to contractions in the Drosophila larval body wall during crawling. Their dendritic branches run along the direction of contraction, possibly a functional requirement to maximise membrane curvature during crawling contractions. Although the molecular machinery of dendritic patterning in c1vpda has been extensively studied, the process leading to the precise elaboration of their comb-like shapes remains elusive. Here, to link dendrite shape with its proprioceptive role, we performed long-term, non-invasive, in vivo time-lapse imaging of c1vpda embryonic and larval morphogenesis to reveal a sequence of differentiation stages. We combined computer models and dendritic branch dynamics tracking to propose that distinct sequential phases of targeted growth and stochastic retraction achieve efficient dendritic trees both in terms of wire and function. Our study shows how dendrite growth balances structure–function requirements, shedding new light on general principles of self-organisation in functionally specialised dendrites.In briefAn optimal wire and function trade-off emerges from noisy growth and stochastic retraction during Drosophila class I ventral posterior dendritic arborisation (c1vpda) dendrite development.HighlightsC1vpda dendrite outgrowth follows wire constraints.Stochastic retraction of functionally suboptimal branches in a subsequent growth phase.C1vpda growth rules favour branches running parallel to larval body wall contraction.Comprehensive growth model reproduces c1vpda development in silico.

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Topical Review: Neuronal Migration in Cortical Development

Journal of Child Neurology ◽

10.1177/08830738040190030201 ◽

2004 ◽

Vol 19 (3) ◽

pp. 274-279

Author(s):

Shigeaki Kanatani ◽

Hidenori Tabata ◽

Kazunori Nakajima

Keyword(s):

Neuronal Migration ◽

Radial Glia ◽

Asymmetric Cell Division ◽

Time Lapse ◽

Radial Glial Cells ◽

Daughter Cells ◽

Radial Glial ◽

Time Lapse Imaging ◽

Mitotic Behavior

Cortical formation in the developing brain is a highly complicated process involving neuronal production (through symmetric or asymmetric cell division) interaction of radial glia with neuronal migration, and multiple modes of neuronal migration. It has been convincingly demonstrated by numerous studies that radial glial cells are neural stem cells. However, the processes by which neurons arise from radial glia and migrate to their final destinations in vivo are not yet fully understood. Recent studies using time-lapse imaging of neuronal migration are giving investigators an increasingly more detailed understanding of the mitotic behavior of radial glia and the migrating behavior of their daughter cells. In this review, we describe recent progress in elucidating neuronal migration in brain formation and how neuronal migration is disturbed by mutations in genes that control this process. ( J Child Neurol 2005;20:274—279).

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Individual neuronal subtypes control initial myelin sheath growth and stabilization

Neural Development ◽

10.1186/s13064-020-00149-3 ◽

2020 ◽

Vol 15 (1) ◽

Author(s):

Heather N. Nelson ◽

Anthony J. Treichel ◽

Erin N. Eggum ◽

Madeline R. Martell ◽

Amanda J. Kaiser ◽

...

Keyword(s):

Spinal Cord ◽

Central Nervous System ◽

Nervous System ◽

Myelin Sheath ◽

Time Lapse ◽

Marked Individual ◽

Larval Zebrafish ◽

Sheath Formation ◽

Time Lapse Imaging

Abstract Background In the developing central nervous system, pre-myelinating oligodendrocytes sample candidate nerve axons by extending and retracting process extensions. Some contacts stabilize, leading to the initiation of axon wrapping, nascent myelin sheath formation, concentric wrapping and sheath elongation, and sheath stabilization or pruning by oligodendrocytes. Although axonal signals influence the overall process of myelination, the precise oligodendrocyte behaviors that require signaling from axons are not completely understood. In this study, we investigated whether oligodendrocyte behaviors during the early events of myelination are mediated by an oligodendrocyte-intrinsic myelination program or are over-ridden by axonal factors. Methods To address this, we utilized in vivo time-lapse imaging in embryonic and larval zebrafish spinal cord during the initial hours and days of axon wrapping and myelination. Transgenic reporter lines marked individual axon subtypes or oligodendrocyte membranes. Results In the larval zebrafish spinal cord, individual axon subtypes supported distinct nascent sheath growth rates and stabilization frequencies. Oligodendrocytes ensheathed individual axon subtypes at different rates during a two-day period after initial axon wrapping. When descending reticulospinal axons were ablated, local spinal axons supported a constant ensheathment rate despite the increased ratio of oligodendrocytes to target axons. Conclusion We conclude that properties of individual axon subtypes instruct oligodendrocyte behaviors during initial stages of myelination by differentially controlling nascent sheath growth and stabilization.

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Regulation of murine copper homeostasis by members of the COMMD protein family

Disease Models & Mechanisms ◽

10.1242/dmm.045963 ◽

2020 ◽

Vol 14 (1) ◽

pp. dmm045963

Author(s):

Amika Singla ◽

Qing Chen ◽

Kohei Suzuki ◽

Jie Song ◽

Alina Fedoseienko ◽

...

Keyword(s):

Copper Homeostasis ◽

Copper Accumulation ◽

Copper Transporter ◽

Copper Excretion ◽

Copper Absorption ◽

Hepatic Copper ◽

High Copper ◽

Molecular Machinery ◽

And Function

ABSTRACTCopper is an essential transition metal for all eukaryotes. In mammals, intestinal copper absorption is mediated by the ATP7A copper transporter, whereas copper excretion occurs predominantly through the biliary route and is mediated by the paralog ATP7B. Both transporters have been shown to be recycled actively between the endosomal network and the plasma membrane by a molecular machinery known as the COMMD/CCDC22/CCDC93 or CCC complex. In fact, mutations in COMMD1 can lead to impaired biliary copper excretion and liver pathology in dogs and in mice with liver-specific Commd1 deficiency, recapitulating aspects of this phenotype. Nonetheless, the role of the CCC complex in intestinal copper absorption in vivo has not been studied, and the potential redundancy of various COMMD family members has not been tested. In this study, we examined copper homeostasis in enterocyte-specific and hepatocyte-specific COMMD gene-deficient mice. We found that, in contrast to effects in cell lines in culture, COMMD protein deficiency induced minimal changes in ATP7A in enterocytes and did not lead to altered copper levels under low- or high-copper diets, suggesting that regulation of ATP7A in enterocytes is not of physiological consequence. By contrast, deficiency of any of three COMMD genes (Commd1, Commd6 or Commd9) resulted in hepatic copper accumulation under high-copper diets. We found that each of these deficiencies caused destabilization of the entire CCC complex and suggest that this might explain their shared phenotype. Overall, we conclude that the CCC complex plays an important role in ATP7B endosomal recycling and function.

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In Vivo Time-Lapse Imaging of Neuronal Development inXenopus

Cold Spring Harbor Protocols ◽

10.1101/pdb.top077156 ◽

2013 ◽

Vol 2013 (9) ◽

pp. pdb.top077156 ◽

Cited By ~ 4

Author(s):

Edward S. Ruthazer ◽

Anne Schohl ◽

Neil Schwartz ◽

Aydin Tavakoli ◽

Marc Tremblay ◽

...

Keyword(s):

Neuronal Development ◽

Time Lapse ◽

Time Lapse Imaging

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Examining seizure-induced effects on the dendritic growth of immature neurons, using in vivo time-lapse imaging of the intact juvenile brain

Clinical Neurophysiology ◽

10.1016/j.clinph.2007.03.028 ◽

2007 ◽

Vol 118 (7) ◽

pp. e186

Author(s):

D. Sesath Hewapathirane ◽

Simon Chen ◽

Wesley Yen ◽

Kurt Haas

Keyword(s):

Dendritic Growth ◽

Time Lapse ◽

Immature Neurons ◽

Time Lapse Imaging

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Sindbis Virus-Induced Neuronal Death Is both Necrotic and Apoptotic and Is Ameliorated byN-Methyl-d-Aspartate Receptor Antagonists

Journal of Virology ◽

10.1128/jvi.75.15.7114-7121.2001 ◽

2001 ◽

Vol 75 (15) ◽

pp. 7114-7121 ◽

Cited By ~ 70

Author(s):

Jennifer L. Nargi-Aizenman ◽

Diane E. Griffin

Keyword(s):

Cell Death ◽

Cortical Neurons ◽

Sindbis Virus ◽

Apoptotic Cell ◽

Time Lapse ◽

Apoptotic Cell Death ◽

Time Lapse Imaging ◽

Alphavirus Infection

ABSTRACT Virus infection of neurons leads to different outcomes ranging from latent and noncytolytic infection to cell death. Viruses kill neurons directly by inducing either apoptosis or necrosis or indirectly as a result of the host immune response. Sindbis virus (SV) is an alphavirus that induces apoptotic cell death both in vitro and in vivo. However, apoptotic changes are not always evident in neurons induced to die by alphavirus infection. Time lapse imaging revealed that SV-infected primary cortical neurons exhibited both apoptotic and necrotic morphological features and that uninfected neurons in the cultures also died. Antagonists of the N-methyl-d-aspartate (NMDA) subtype of glutamate receptors protected neurons from SV-induced death without affecting virus replication or SV-induced apoptotic cell death. These results provide evidence that SV infection activates neurotoxic pathways that result in aberrant NMDA receptor stimulation and damage to infected and uninfected neurons.

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In vivo Postnatal Electroporation and Time-lapse Imaging of Neuroblast Migration in Mouse Acute Brain Slices

Journal of Visualized Experiments ◽

10.3791/50905 ◽

2013 ◽

Cited By ~ 6

Author(s):

Martina Sonego ◽

Ya Zhou ◽

Madeleine Julie Oudin ◽

Patrick Doherty ◽

Giovanna Lalli

Keyword(s):

Brain Slices ◽

Time Lapse ◽

Neuroblast Migration ◽

Time Lapse Imaging

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In vivo single cell analysis reveals Gata2 dynamics in cells transitioning to hematopoietic fate

Journal of Experimental Medicine ◽

10.1084/jem.20170807 ◽

2017 ◽

Vol 215 (1) ◽

pp. 233-248 ◽

Cited By ~ 17

Author(s):

Christina Eich ◽

Jochen Arlt ◽

Chris S. Vink ◽

Parham Solaimani Kartalaei ◽

Polynikis Kaimakis ◽

...

Keyword(s):

Transcription Factor ◽

Cell Fate ◽

Regulatory Networks ◽

Single Cell Analysis ◽

Single Cells ◽

Time Lapse ◽

Hematopoietic Stem ◽

And Function ◽

In Cells

Cell fate is established through coordinated gene expression programs in individual cells. Regulatory networks that include the Gata2 transcription factor play central roles in hematopoietic fate establishment. Although Gata2 is essential to the embryonic development and function of hematopoietic stem cells that form the adult hierarchy, little is known about the in vivo expression dynamics of Gata2 in single cells. Here, we examine Gata2 expression in single aortic cells as they establish hematopoietic fate in Gata2Venus mouse embryos. Time-lapse imaging reveals rapid pulsatile level changes in Gata2 reporter expression in cells undergoing endothelial-to-hematopoietic transition. Moreover, Gata2 reporter pulsatile expression is dramatically altered in Gata2+/− aortic cells, which undergo fewer transitions and are reduced in hematopoietic potential. Our novel finding of dynamic pulsatile expression of Gata2 suggests a highly unstable genetic state in single cells concomitant with their transition to hematopoietic fate. This reinforces the notion that threshold levels of Gata2 influence fate establishment and has implications for transcription factor–related hematologic dysfunctions.

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