Neurodegeneration in a novel invertebrate model system: Failed microtubule‐mediated cell adhesion and unraveling of macroglia

Neurodegeneration in a novel invertebrate model system: Failed microtubule‐mediated cell adhesion and unraveling of macroglia

Neurodegenerative diseases are among the main causes of death in the United States, leading to irreversible disintegration of neurons. Despite intense international research efforts, cellular mechanisms that initiate neurodegeneration remain elusive, thus inhibiting the development of effective prev...

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Published in:Journal of comparative neurology (1911) Vol. 531; no. 5; pp. 618 - 638
Main Authors: Fabian‐Fine, Ruth, Aiken, Anna M., Aug, Julia R., Boucher, Jason D., Butler, Danielle C., Clancy, Liam J., Clem, Shaun A., Crotty, Samantha C., Dalpe, Abigail M., Donzello‐Jewett, Elizabeth J., Galgay, Taylor M., Gillis, Bonnie K., Heinrich, Brigid W., Hines, Kai R., Kimmel, Jordan E., McGrath, Joseph M., Miles, Marissa M., Morey, Jordyn A., Ortiz, Isaiah A., Pham, Kevin Q., Quinn, Liam C., Radican, Colin J., Speidel, Nolan T., Thomas, Bailey J., Troisi, Angela R., Weiss, Joshua L., Wentzheimer, Kayne V., Weaver, Adam L.
Format: Journal Article
Language:English
Published: United States Wiley Subscription Services, Inc 01-04-2023
Subjects:
Animals
Brain
Cell Adhesion
Cupiennius salei
desmosomes
Glia
Invertebrates
macroglia
Mammals
Medical treatment
Microtubules
Neurodegeneration
Neurodegenerative diseases
Neuronal-glial interactions
Neurons - metabolism
Spiders
Toluidine
macroglia
desmosomes
microtubules
Cupiennius salei
cell adhesion
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Summary:Neurodegenerative diseases are among the main causes of death in the United States, leading to irreversible disintegration of neurons. Despite intense international research efforts, cellular mechanisms that initiate neurodegeneration remain elusive, thus inhibiting the development of effective preventative and early onset medical treatment. To identify underlying cellular mechanisms that initiate neuron degeneration, it is critical to identify histological and cellular hallmarks that can be linked to underlying biochemical processes. Due to the poor tissue preservation of degenerating mammalian brain tissue, our knowledge regarding histopathological hallmarks of early to late degenerative stages is only fragmentary. Here, we introduce a novel model organism to study histological hallmarks of neurodegeneration, the spider Cupiennius salei. We utilized toluidine blue‐stained 0.9‐μm serial semithin and 50‐nm ultrathin sections of young and old spider nervous tissue. Our findings suggest that the initial stages of neurodegeneration in spiders may be triggered by (1) dissociation of neuron‐ and glia‐derived microtubules, and (2) the weakening of microtubule‐associated desmosomal junctions that lead to the unraveling of neuron‐insulating macroglia, compromising the structural integrity of affected neurons. The involvement of macroglia in the disposal of neuronal debris described here—although different in the proposed transport mechanisms—shows resemblance to the mammalian glymphatic system. We propose that this model system is highly suitable to investigate invertebrate neurodegenerative processes from early onset to scar formation and that this knowledge may be useful for the study of neurodegeneration in mammalian tissue. Early stages of neurodegeneration in the spider, Cupiennius salei, show unraveling of macroglia around neurons, which is likely due to the catastrophic failure of microtubule‐associated desmosomes. This unraveling is followed by the depletion of neuronal cytoplasmic content into the unraveling macroglia, inducing cell death of both neurons and glia cells.
Bibliography:Anna M. Aiken, Julia R. Aug, Jason D. Boucher, Danielle C. Butler, Liam J. Clancy, Shaun A. Clem, Samantha C. Crotty, Abigail M. Dalpe, Elizabeth J. Donzello‐Jewett, Taylor M. Galgay, Bonnie K. Gillis, Brigid W. Heinrich, Kai R. Hines, Jordan E. Kimmel, Joseph M. McGrath, Marissa M. Miles, Jordyn A. Morey, Isaiah A. Ortiz, Kevin Q. Pham, Liam C. Quinn, Colin J. Radican, Nolan T. Speidel, Bailey J. Thomas, Angela R. Troisi, Joshua L. Weiss, and Kayne V. Wentzheimer are students of the Cellular/Molecular Research Classes 2021 and 2022.
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AUTHOR CONTRIBUTIONS
Ruth Fabian-Fine designed the experiments, performed the experiments, analyzed the data, drafted the manuscript, and edited the manuscript. Anna M. Aiken, Julia R. Aug, Jason D. Boucher, Danielle C. Butler, Liam J. Clancy, Shaun A. Clem, Samantha C. Crotty, Abigail M. Dalpe, Elizabeth J. Donzello-Jewett, Taylor M. Galgay, Bonnie K. Gillis, Brigid W. Heinrich, Kai R. Hines, Jordan E. Kimmel, Joseph M. McGrath, Marissa M. Miles, Jordyn A. Morey, Isaiah A. Ortiz, Kevin Q. Pham, Liam C. Quinn, Colin J. Radican, Nolan T. Speidel, Bailey J. Thomas, Angela R. Troisi, Joshua L. Weiss, and Kayne V. Wentzheimer performed the experiments and analyzed the data. Adam Weaver designed the experiments, performed the experiments, analyzed the data, and edited the manuscript.
ISSN:0021-9967
1096-9861
DOI:10.1002/cne.25450