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Article ; Online: Echinoderm radial glia in adult cell renewal, indeterminate growth, and regeneration.

Mashanov, Vladimir / Ademiluyi, Soji / Jacob Machado, Denis / Reid, Robert / Janies, Daniel

2023 Volume 17, Page(s) 1258370

Abstract: Echinoderms are a phylum of marine deterostomes with a range of interesting biological features. One remarkable ability is their impressive capacity to regenerate most of their adult tissues, including the central nervous system (CNS). The research ... ...

Abstract	Echinoderms are a phylum of marine deterostomes with a range of interesting biological features. One remarkable ability is their impressive capacity to regenerate most of their adult tissues, including the central nervous system (CNS). The research community has accumulated data that demonstrates that, in spite of the pentaradial adult body plan, echinoderms share deep similarities with their bilateral sister taxa such as hemichordates and chordates. Some of the new data reveal the complexity of the nervous system in echinoderms. In terms of the cellular architecture, one of the traits that is shared between the CNS of echinoderms and chordates is the presence of radial glia. In chordates, these cells act as the main progenitor population in CNS development. In mammals, radial glia are spent in embryogenesis and are no longer present in adults, being replaced with other neural cell types. In non-mammalian chordates, they are still detected in the mature CNS along with other types of glia. In echinoderms, radial glia also persist into the adulthood, but unlike in chordates, it is the only known glial cell type that is present in the fully developed CNS. The echinoderm radial glia is a multifunctional cell type. Radial glia forms the supporting scaffold of the neuroepithelium, exhibits secretory activity, clears up dying or damaged cells by phagocytosis, and, most importantly, acts as a major progenitor cell population. The latter function is critical for the outstanding developmental plasticity of the adult echinoderm CNS, including physiological cell turnover, indeterminate growth, and a remarkable capacity to regenerate major parts following autotomy or traumatic injury. In this review we summarize the current knowledge on the organization and function of the echinoderm radial glia, with a focus on the role of this cell type in adult neurogenesis.
MeSH term(s)	Animals ; Ependymoglial Cells ; Echinodermata/physiology ; Neuroglia/metabolism ; Neurons ; Neurogenesis/physiology ; Mammals
Language	English
Publishing date	2023-09-29
Publishing country	Switzerland
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural
ZDB-ID	2452968-0
ISSN	1662-5110 ; 1662-5110
ISSN (online)	1662-5110
ISSN	1662-5110
DOI	10.3389/fncir.2023.1258370
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Protein storage and reproduction increase in grasshoppers on a diet matched to the amino acids of egg yolk protein.

Hatle, John D / Maslikova, Victoriya / Short, Clancy A / Bracey, Donald / Darmanjian, Margaret / Morningstar, Sarah / Reams, Brooke / Mashanov, Vladimir S / Jahan-Mihan, Alireza / Hahn, Daniel A

The Journal of experimental biology

2022 Volume 225, Issue 17

Abstract: The diets of animals are essential to support development, and protein is key. Accumulation of stored nutrients can support developmental events such as molting and initiation of reproduction. Agricultural studies have addressed how dietary protein ... ...

Abstract	The diets of animals are essential to support development, and protein is key. Accumulation of stored nutrients can support developmental events such as molting and initiation of reproduction. Agricultural studies have addressed how dietary protein quality affects growth, but few studies have addressed the effects of dietary protein quality on developmental transitions. Studies on how dietary quality may affect protein storage and development are possible in arthropods, which store proteins in the hemolymph. We hypothesized that diets with a composition of amino acids that matches the precursor of egg yolk protein (vitellogenin, Vg) will be high quality and support both egg production and accumulation of storage proteins. Grasshoppers were fed one of two isonitrogenous solutions of amino acids daily: Vg-balanced (matched to Vg) or Unbalanced (same total moles of amino acids, but not matched to egg yolk). We measured reproduction and storage protein levels in serial hemolymph samples from individuals. The Vg-balanced group had greater reproduction and greater cumulative levels of storage proteins than did the Unbalanced group. This occurred even though amino acids fed to the Vg-balanced group were not a better match to storage protein than were the amino acids fed to the Unbalanced group. Further, oviposition timing was best explained by a combination of diet, age at the maximum level of storage protein hexamerin-270 and accumulation of hexamerin-90. Our study tightens the link between storage proteins and commitment to reproduction, and shows that dietary protein quality is vital for protein storage and reproduction.
MeSH term(s)	Amino Acids/metabolism ; Animal Feed ; Animals ; Diet ; Egg Proteins/metabolism ; Egg Yolk/chemistry ; Female ; Grasshoppers/metabolism ; Reproduction
Chemical Substances	Amino Acids ; Egg Proteins
Language	English
Publishing date	2022-09-07
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	218085-6
ISSN	1477-9145 ; 0022-0949
ISSN (online)	1477-9145
ISSN	0022-0949
DOI	10.1242/jeb.244450
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Article: Draft Genome of the Sea Cucumber

Medina-Feliciano, Joshua G / Pirro, Stacy / García-Arrarás, Jose E / Mashanov, Vladimir / Ryan, Joseph F

Frontiers in Marine Science

2021 Volume 8

Abstract: Regeneration is one of the most fascinating and yet least understood biological processes. Echinoderms, one of the closest related invertebrate groups to humans, can contribute to our understanding of the genetic basis of regenerative processes. Among ... ...

Abstract	Regeneration is one of the most fascinating and yet least understood biological processes. Echinoderms, one of the closest related invertebrate groups to humans, can contribute to our understanding of the genetic basis of regenerative processes. Among echinoderms, sea cucumbers have the ability to grow back most of their body parts following injury, including the intestine and nervous tissue. The cellular and molecular events underlying these abilities in sea cucumbers have been most extensively studied in the species
Language	English
Publishing date	2021-04-15
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2757748-X
ISSN	2296-7745
ISSN	2296-7745
DOI	10.3389/fmars.2021.603410
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Article: Inhibition of cell proliferation does not slow down echinoderm neural regeneration.

Mashanov, Vladimir S / Zueva, Olga R / García-Arrarás, José E

Frontiers in zoology

2017 Volume 14, Page(s) 12

Abstract: Background: Regeneration of the damaged central nervous system is one of the most interesting post-embryonic developmental phenomena. Two distinct cellular events have been implicated in supplying regenerative neurogenesis with cellular material - ... ...

Abstract	Background: Regeneration of the damaged central nervous system is one of the most interesting post-embryonic developmental phenomena. Two distinct cellular events have been implicated in supplying regenerative neurogenesis with cellular material - generation of new cells through cell proliferation and recruitment of already existing cells through cell migration. The relative contribution and importance of these two mechanisms is often unknown. Methods: Here, we use the regenerating radial nerve cord (RNC) of the echinoderm Results: Aphidicolin treatment resulted in a significant 2.1-fold decrease in cell proliferation. In spite of this, the regenerating RNC in the treated animals did not differ in histological architecture, size and cell number from its counterpart in the control vehicle-treated animals. DiI labeling showed extensive cell migration in the RNC. Some cells migrated from as far as 2 mm away from the injury plane to contribute to the neural outgrowth. Conclusions: We suggest that inhibition of cell division in the regenerating RNC of
Language	English
Publishing date	2017-02-23
Publishing country	England
Document type	Journal Article
ISSN	1742-9994
ISSN	1742-9994
DOI	10.1186/s12983-017-0196-y
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Article ; Online: Postembryonic organogenesis of the digestive tube: why does it occur in worms and sea cucumbers but fail in humans?

Mashanov, Vladimir S / Zueva, Olga / García-Arrarás, José E

Current topics in developmental biology

2014 Volume 108, Page(s) 185–216

Abstract: We provide an integrative view of mechanisms that enable regeneration of the digestive tube in various animal models, including vertebrates, tunicates, echinoderms, insects, and flatworms. Two main strategies of regeneration of the endodermal luminal ( ... ...

Abstract	We provide an integrative view of mechanisms that enable regeneration of the digestive tube in various animal models, including vertebrates, tunicates, echinoderms, insects, and flatworms. Two main strategies of regeneration of the endodermal luminal (mucosal) epithelium have evolved in metazoans. One of them involves proliferation of resident epithelial cells, while the other relies on recruitment of cells from extramucosal sources. In any of these two scenarios, either pluri-/multipotent stem cells or specialized differentiated cells can be used as the starting material. Posttraumatic visceral regeneration shares some common mechanisms with normal embryonic development as well as with organ homeostatic maintenance, but there are signaling pathways and/or cellular pools that are specific to the regenerative phenomena. Comparative analysis of the literature suggests that mammals share with spontaneously regenerating animals many of the regeneration-related adaptations and are able to efficiently repair components of their digestive tube at the level of individual tissues, but fail to do so at the whole-organ scale. We review what might cause this failure in the context of the current state of knowledge about various regenerative models.
MeSH term(s)	Animals ; Cell Differentiation ; Echinodermata/growth & development ; Gastrointestinal Tract/growth & development ; Humans ; Intestines/growth & development ; Platyhelminths/growth & development ; Regeneration/physiology ; Sea Cucumbers/growth & development ; Signal Transduction ; Stem Cells/cytology ; Urochordata/growth & development
Language	English
Publishing date	2014-02-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ISSN	1557-8933 ; 0070-2153
ISSN (online)	1557-8933
ISSN	0070-2153
DOI	10.1016/B978-0-12-391498-9.00006-1
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Article: Inhibition of cell proliferation does not slow down echinoderm neural regeneration

Mashanov, VladimirS / Zueva, OlgaR / García-Arrarás, JoséE

Frontiers in zoology. 2017 Dec., v. 14, no. 1

2017

Abstract: ... regenerating animals with aphidicolin, a specific inhibitor of S-phase DNA replication. To monitor the effect ...

Abstract	BACKGROUND: Regeneration of the damaged central nervous system is one of the most interesting post-embryonic developmental phenomena. Two distinct cellular events have been implicated in supplying regenerative neurogenesis with cellular material – generation of new cells through cell proliferation and recruitment of already existing cells through cell migration. The relative contribution and importance of these two mechanisms is often unknown. METHODS: Here, we use the regenerating radial nerve cord (RNC) of the echinoderm Holothuria glaberrima as a model of extensive post-traumatic neurogenesis in the deuterostome central nervous system. To uncouple the effects of cell proliferation from those of cell migration, we treated regenerating animals with aphidicolin, a specific inhibitor of S-phase DNA replication. To monitor the effect of aphidicolin on DNA synthesis, we used BrdU immunocytochemistry. The specific radial glial marker ERG1 was used to label the regenerating RNC. Cell migration was tracked with vital staining with the lipophilic dye DiI. RESULTS: Aphidicolin treatment resulted in a significant 2.1-fold decrease in cell proliferation. In spite of this, the regenerating RNC in the treated animals did not differ in histological architecture, size and cell number from its counterpart in the control vehicle-treated animals. DiI labeling showed extensive cell migration in the RNC. Some cells migrated from as far as 2 mm away from the injury plane to contribute to the neural outgrowth. CONCLUSIONS: We suggest that inhibition of cell division in the regenerating RNC of H. glaberrima is compensated for by recruitment of cells, which migrate into the RNC outgrowth from deeper regions of the neuroepithelium. Neural regeneration in echinoderms is thus a highly regulative developmental phenomenon, in which the size of the cell pool can be controlled either by cell proliferation or cell migration, and the latter can neutralize perturbations in the former.
Keywords	DNA replication ; Holothuria ; animals ; cell division ; cell movement ; cell proliferation ; central nervous system ; enzyme inhibitors ; histology ; immunocytochemistry ; models ; nerve tissue ; neurogenesis ; neutralization ; staining
Language	English
Dates of publication	2017-12
Size	p. 12.
Publishing place	BioMed Central
Document type	Article
ISSN	1742-9994
DOI	10.1186/s12983-017-0196-y
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Article ; Online: Myc regulates programmed cell death and radial glia dedifferentiation after neural injury in an echinoderm.

Mashanov, Vladimir S / Zueva, Olga R / García-Arrarás, José E

BMC developmental biology

2015 Volume 15, Page(s) 24

Abstract: ... factor, whose expression significantly increased in the wounded CNS. The specific function(s ...

Abstract	Background: Adult echinoderms can completely regenerate major parts of their central nervous system even after severe injuries. Even though this capacity has long been known, the molecular mechanisms that drive fast and complete regeneration in these animals have remained uninvestigated. The major obstacle for understanding these molecular pathways has been the lack of functional genomic studies on regenerating adult echinoderms. Results: Here, we employ RNA interference-mediated gene knockdown to characterize the role of Myc during the early (first 48 hours) post-injury response in the radial nerve cord of the sea cucumber Holothuria glaberrima. Our previous experiments identified Myc as the only pluripotency-associated factor, whose expression significantly increased in the wounded CNS. The specific function(s) of this gene, however, remained unknown. Here we demonstrate that knockdown of Myc inhibits dedifferentiation of radial glia and programmed cell death, the two most prominent cellular events that take place in the regenerating sea cucumber nervous system shortly after injury. Conclusions: In this study, we show that Myc overexpression is required for proper dedifferentiation of radial glial cells and for triggering the programmed cell death in the vicinity of the injury. Myc is thus the first transcription factor, whose functional role has been experimentally established in echinoderm regeneration.
MeSH term(s)	Animals ; Apoptosis/physiology ; Cell Differentiation ; Echinodermata ; Electroporation ; Gene Knockdown Techniques ; Genes, myc ; Neuroglia/cytology ; RNA Interference ; RNA, Messenger/genetics ; Radial Nerve/injuries
Chemical Substances	RNA, Messenger
Language	English
Publishing date	2015-05-30
Publishing country	England
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.
ISSN	1471-213X
ISSN (online)	1471-213X
DOI	10.1186/s12861-015-0071-z
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Article: Heterogeneous generation of new cells in the adult echinoderm nervous system.

Mashanov, Vladimir S / Zueva, Olga R / García-Arrarás, José E

Frontiers in neuroanatomy

2015 Volume 9, Page(s) 123

Abstract: Adult neurogenesis, generation of new functional cells in the mature central nervous system (CNS), has been documented in a number of diverse organisms, ranging from humans to invertebrates. However, the origin and evolution of this phenomenon is still ... ...

Abstract	Adult neurogenesis, generation of new functional cells in the mature central nervous system (CNS), has been documented in a number of diverse organisms, ranging from humans to invertebrates. However, the origin and evolution of this phenomenon is still poorly understood for many of the key phylogenetic groups. Echinoderms are one such phylum, positioned as a sister group to chordates within the monophyletic clade Deuterostomia. They are well known for the ability of their adult organs, including the CNS, to completely regenerate after injury. Nothing is known, however, about production of new cells in the nervous tissue under normal physiological conditions in these animals. In this study, we show that new cells are continuously generated in the mature radial nerve cord (RNC) of the sea cucumber Holothuria glaberrima. Importantly, this neurogenic activity is not evenly distributed, but is significantly more extensive in the lateral regions of the RNC than along the midline. Some of the new cells generated in the apical region of the ectoneural neuroepithelium leave their place of origin and migrate basally to populate the neural parenchyma. Gene expression analysis showed that generation of new cells in the adult sea cucumber CNS is associated with transcriptional activity of genes known to be involved in regulation of various aspects of neurogenesis in other animals. Further analysis of one of those genes, the transcription factor Myc, showed that it is expressed, in some, but not all radial glial cells, suggesting heterogeneity of this CNS progenitor cell population in echinoderms.
Language	English
Publishing date	2015-09-22
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452969-2
ISSN	1662-5129
ISSN	1662-5129
DOI	10.3389/fnana.2015.00123
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Article ; Online: Expression of pluripotency factors in echinoderm regeneration.

Mashanov, Vladimir S / Zueva, Olga R / García-Arrarás, José E

Cell and tissue research

2015 Volume 359, Issue 2, Page(s) 521–536

Abstract: Cell dedifferentiation is an integral component of post-traumatic regeneration in echinoderms. As dedifferentiated cells become multipotent, we asked if this spontaneous broadening of developmental potential is associated with the action of the same ... ...

Abstract	Cell dedifferentiation is an integral component of post-traumatic regeneration in echinoderms. As dedifferentiated cells become multipotent, we asked if this spontaneous broadening of developmental potential is associated with the action of the same pluripotency factors (known as Yamanaka factors) that were used to induce pluripotency in specialized mammalian cells. In this study, we investigate the expression of orthologs of the four Yamanaka factors in regeneration of two different organs, the radial nerve cord and the digestive tube, in the sea cucumber Holothuria glaberrima. All four pluripotency factors are expressed in uninjured animals, although their expression domains do not always overlap. In regeneration, the expression levels of the four genes were not regulated in a coordinated way, but instead showed different dynamics for individual genes and also were different between the radial nerve and the gut. SoxB1, the ortholog of the mammalian Sox2, was drastically downregulated in the regenerating intestine, suggesting that this factor is not required for dedifferentiation/regeneration in this organ. On the other hand, during the early post-injury stage, Myc, the sea cucumber ortholog of c-Myc, was significantly upregulated in both the intestine and the radial nerve cord and is therefore hypothesized to play a central role in dedifferentiation/regeneration of various tissue types.
MeSH term(s)	Animals ; Evolution, Molecular ; Gene Expression Regulation ; Holothuria/physiology ; Nerve Regeneration/physiology ; Phylogeny ; Pluripotent Stem Cells/metabolism ; Protein Structure, Tertiary ; Regeneration ; Sequence Homology, Amino Acid ; Time Factors ; Transcription Factors/chemistry ; Transcription Factors/metabolism
Chemical Substances	Transcription Factors
Language	English
Publishing date	2015-02
Publishing country	Germany
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	125067-x
ISSN	1432-0878 ; 0302-766X
ISSN (online)	1432-0878
ISSN	0302-766X
DOI	10.1007/s00441-014-2040-4
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Article: Expression of pluripotency factors in echinoderm regeneration

Mashanov, Vladimir S / Zueva, Olga R / García-Arrarás, José E

Cell and tissue research. 2015 Feb., v. 359, no. 2

2015

Abstract	Cell dedifferentiation is an integral component of post-traumatic regeneration in echinoderms. As dedifferentiated cells become multipotent, we asked if this spontaneous broadening of developmental potential is associated with the action of the same pluripotency factors (known as Yamanaka factors) that were used to induce pluripotency in specialized mammalian cells. In this study, we investigate the expression of orthologs of the four Yamanaka factors in regeneration of two different organs, the radial nerve cord and the digestive tube, in the sea cucumber Holothuria glaberrima. All four pluripotency factors are expressed in uninjured animals, although their expression domains do not always overlap. In regeneration, the expression levels of the four genes were not regulated in a coordinated way, but instead showed different dynamics for individual genes and also were different between the radial nerve and the gut. SoxB1, the ortholog of the mammalian Sox2, was drastically downregulated in the regenerating intestine, suggesting that this factor is not required for dedifferentiation/regeneration in this organ. On the other hand, during the early post-injury stage, Myc, the sea cucumber ortholog of c-Myc, was significantly upregulated in both the intestine and the radial nerve cord and is therefore hypothesized to play a central role in dedifferentiation/regeneration of various tissue types.
Keywords	Holothuria ; cell dedifferentiation ; digestive system ; genes ; mammals ; nerve tissue
Language	English
Dates of publication	2015-02
Size	p. 521-536.
Publishing place	Springer-Verlag
Document type	Article
ZDB-ID	125067-x
ISSN	1432-0878 ; 0302-766X
ISSN (online)	1432-0878
ISSN	0302-766X
DOI	10.1007/s00441-014-2040-4
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