scholarly journals The neuron pioneering the ventral nerve cord does not follow the common pathway of neurogenesis in the polychaete Malacoceros fuliginosus

2020 ◽  
Author(s):  
Suman Kumar ◽  
Sharat Chandra Tumu ◽  
Conrad Helm ◽  
Harald Hausen

Abstract Background: Nervous system development is an interplay of many processes: the formation of individual neurons which depends on whole-body and local patterning processes and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is increasing, data on pioneer neurons that create the early axonal scaffold are scarce. Here we studied the early steps of nervous system development in the annelid Malacoceros fuliginosus.Results: We find that the first pioneer neurons are already in place in the anterior and posterior pole when broad neurogenesis is just starting. They do not express serotonin or FMRFamide which are commonly used markers in studies on nervous system architecture. A single posterior neuron prefigures the main course of the ventral nerve cord and this mode is probably ancestral for majority of annelids. Notably, none of the studied sox and proneural genes, which are commonly involved in the generation of neurons, is expressed by this important neuron. The only transcription factor we found expressed is Brn3, which likely acts on a low hierarchical level.Conclusions: We propose that the annelid ventral nerve cord pioneer neuron follows a highly divergent course of neurogenesis. The lack of Sox and proneural transcription factors, which are usually under control of patterning cell-extrinsic factors suggest a major influence of inherited cell-intrinsic properties on the development of this cell. Though cell-autonomous specification is generally an important pathway in the early development of spirally cleaving animals, its relevance for nervous system development is poorly understood. Our data suggest that closer investigation of the specification of pioneer neurons in animals featuring spiral cleavage will be highly informative to obtain a better understanding of how nervous systems form and evolve.

2020 ◽  
Author(s):  
Suman Kumar ◽  
Sharat Chandra Tumu ◽  
Conrad Helm ◽  
Harald Hausen

Abstract Background Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is increasing, data on pioneer neurons that create the early axonal scaffold are scarce. Here we studied the first steps of nervous system development in the annelid Malacoceros fuliginosus . Results Here, we performed a dense expression profiling of a broad set of neural genes. We found that SoxB expression begins at 4 hours postfertilization, and shortly later, the neuronal progenitors can be identified at the anterior and the posterior pole by the transient and dynamic expression of proneural genes. At 9 hpf, the first neuronal cells start differentiating, and we provide a detailed description of axonal outgrowth of the pioneer neurons that create the primary neuronal scaffold. Tracing back the clonal origin of the ventral nerve cord pioneer neuron revealed that it is a descendant of the blastomere 2d (2d 221 ), which after 7 cleavages starts expressing Neurogenin , Achaete-Scute and NeuroD . Conclusions We propose that an anterior and posterior origin of the nervous system is ancestral in annelids. The specification of the relevant neurons starts very early and we suggest that closer examination of the first pioneer neurons will be valuable in better understanding of nervous system development in spirally cleaving animals, to determine the potential role of cell-intrinsic properties in neuronal specification and to resolve the evolution of nervous systems.


2020 ◽  
Vol 20 (1) ◽  
Author(s):  
Suman Kumar ◽  
Sharat Chandra Tumu ◽  
Conrad Helm ◽  
Harald Hausen

Abstract Background Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is increasing, data on pioneer neurons that create the early axonal scaffold are scarce. Here we studied the first steps of nervous system development in the annelid Malacoceros fuliginosus. Results We performed a dense expression profiling of a broad set of neural genes. We found that SoxB expression begins at 4 h postfertilization, and shortly later, the neuronal progenitors can be identified at the anterior and the posterior pole by the transient and dynamic expression of proneural genes. At 9 hpf, the first neuronal cells start differentiating, and we provide a detailed description of axonal outgrowth of the pioneer neurons that create the primary neuronal scaffold. Tracing back the clonal origin of the ventral nerve cord pioneer neuron revealed that it is a descendant of the blastomere 2d (2d221), which after 7 cleavages starts expressing Neurogenin, Acheate-Scute and NeuroD. Conclusions We propose that an anterior and posterior origin of the nervous system is ancestral in annelids. We suggest that closer examination of the first pioneer neurons will be valuable in better understanding of nervous system development in spirally cleaving animals, to determine the potential role of cell-intrinsic properties in neuronal specification and to resolve the evolution of nervous systems.


Development ◽  
1997 ◽  
Vol 124 (13) ◽  
pp. 2571-2580 ◽  
Author(s):  
B. Wightman ◽  
R. Baran ◽  
G. Garriga

During nervous system development, growth cone pioneering and fasciculation contribute to nerve bundle structure. Pioneer growth cones initially navigate along neuroglia to establish an axon scaffold that guides later extending growth cones. In C. elegans, the growth cone of the PVPR neuron pioneers the left ventral nerve cord bundle, providing a path for the embryonic extensions of the PVQL and AVKR growth cones. Later during larval development, the HSNL growth cone follows cues in the left ventral nerve cord bundle provided by the PVPR and PVQL axons. Here we show that mutations in the genes enu-1, fax-1, unc-3, unc-30, unc-42 and unc-115 disrupt pathfinding of growth cones along the left ventral nerve cord bundle. Our results indicate that unc-3 and unc-30 function in ventral nerve cord pioneering and that enu-1, fax-1, unc-42 and unc-115 function in recognition of the PVPR and PVQL axons by the AVKR and HSNL growth cones.


2020 ◽  
Author(s):  
Elizaveta Fofanova ◽  
Tatiana Mayorova ◽  
Elena Voronezhskaya

Abstract BackgroundThe structure and development of the nervous system in Lophotrochozoa species is of the most important questions for comparative neurobiology. During the last decade the number of comprehensive studies on the development of serotonergic and FMRFamidergic systems has been skyrocketing. However, the detailed research of the earliest events of Polychaeta neurogenesis is still sparce. Polychaeta is a huge taxon within Lophotrochozoa. Its representatives are widely used as model systems in developmental and physiological investigations. Dinophilidae is a unique Polychaeta group. Its representatives combine morphological traits of different lophotrochozoan taxa. Moreover, adult dinophilids demonstrate morphological similarity to a trochophore larva. This similarity may be associated with either archaic origin of this group or neoteny. The main goal of our study is to provide a detailed description of the earliest events in Dinophilus neurogenesis. These data might improve our understanding of Polychaeta development and evolution.ResultsWe have studied the earliest events in nervous system development in two relative species D. gyrociliatus and D. taeniatus using immunochemical labelling of serotonin, FMRF-amide related peptides, and acetylated tubulin. We used external ciliation as marker for staging. Both species go through the same developmental stages: prototroch, ventral ciliary field and ciliary bands. In both species the first neurons differenciate revealed by anti alpha-acetylated tubulin antibodies only and show no reaction with 5-HT or FMRFa antibodies. These neurons located at the anterior and posterior parts of the embryo in both species. In D. taeniatus embryons the anterior cell is transient and disappear just after head neuropil is constructed. On the contrary, in D. gyrociliatus embryos the anterior cell is not transient and remains at the same position during the whole life span of the specimen. Caudal cell is present during the whole embryogenesis in both species. Neurites of these early neurons surround the stomadeum and constitute anlagen of paired ventro-lateral longitudinal bundles. During the development the number of neurites increases and they form compact head neuropil, paired ventro-lateral and lateral longitudinal bundles, unpaired medial longitudinal bundle and transverse commissures in ventral hyposphere. Serotonin- and FMRFamide-immunoreactive neurons differentiate adjacent to ventro-lateral bundles and head neuropil, respectively, after the establishment of main structures of the nervous system at the ventral ciliary field and ciliary bands stages. Processes of serotonin-, FMRFamide- immunopositive neurons constitute the small portion of tubulin immunopositive neuropil at all described stages.ConclusionsWe announce a detailed data on the earliest events in D. gyrociliatus and D. taeniatus neurodevelopment based on anti-acetylated tubulin, serotonin, and FMRFamide-like immuno labeling. The first nerve elements demonstrate no 5-HT-IR and no FMRFa-IR, which differs from the most Polychaetes and even Lophotrochozoans, investigated so far. Moreover, these animals do not have a typical apical organ (or perhaps do not have it at all) and the pioneer neurons of D.gyrociliatus are also peculiar in that they join the definitive nervous system unlike other lophotrochozoans where pioneer nerons are transient. Thus, Dinophilus neurogenesis demonstrates a variation of common scheme. The reported study was funded by RFBR, project number 19-3460040.


2013 ◽  
Vol 14 (2) ◽  
pp. 160-166
Author(s):  
Diego Gazzolo ◽  
Laura D. Serpero ◽  
Alessandro Frigiola ◽  
Raul Abella ◽  
Alessandro Giamberti ◽  
...  

Cells ◽  
2021 ◽  
Vol 10 (6) ◽  
pp. 1453
Author(s):  
Joaquín Martí-Clúa

The synthetic halogenated pyrimidine analog, 5-bromo-2′-deoxyuridine (BrdU), is a marker of DNA synthesis. This exogenous nucleoside has generated important insights into the cellular mechanisms of the central nervous system development in a variety of animals including insects, birds, and mammals. Despite this, the detrimental effects of the incorporation of BrdU into DNA on proliferation and viability of different types of cells has been frequently neglected. This review will summarize and present the effects of a pulse of BrdU, at doses ranging from 25 to 300 µg/g, or repeated injections. The latter, following the method of the progressively delayed labeling comprehensive procedure. The prenatal and perinatal development of the cerebellum are studied. These current data have implications for the interpretation of the results obtained by this marker as an index of the generation, migration, and settled pattern of neurons in the developing central nervous system. Caution should be exercised when interpreting the results obtained using BrdU. This is particularly important when high or repeated doses of this agent are injected. I hope that this review sheds light on the effects of this toxic maker. It may be used as a reference for toxicologists and neurobiologists given the broad use of 5-bromo-2′-deoxyuridine to label dividing cells.


2021 ◽  
Vol 81 (3) ◽  
pp. 229-230
Author(s):  
Frank Bradke ◽  
Antonina Roll‐Mecak

Neuroforum ◽  
2021 ◽  
Vol 0 (0) ◽  
Author(s):  
Christoph Giez ◽  
Alexander Klimovich ◽  
Thomas C. G. Bosch

Abstract Animals have evolved within the framework of microbes and are constantly exposed to diverse microbiota. Microbes colonize most, if not all, animal epithelia and influence the activity of many organs, including the nervous system. Therefore, any consideration on nervous system development and function in the absence of the recognition of microbes will be incomplete. Here, we review the current knowledge on the nervous systems of Hydra and its role in the host–microbiome communication. We show that recent advances in molecular and imaging methods are allowing a comprehensive understanding of the capacity of such a seemingly simple nervous system in the context of the metaorganism. We propose that the development, function and evolution of neural circuits must be considered in the context of host–microbe interactions and present Hydra as a strategic model system with great basic and translational relevance for neuroscience.


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