scholarly journals Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia

BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Ludwik Gąsiorowski ◽  
Aina Børve ◽  
Irina A. Cherneva ◽  
Andrea Orús-Alcalde ◽  
Andreas Hejnol
Keyword(s):  
Neural Development ◽  
Evolutionary Process ◽  
Cell Types ◽  
Major Elements ◽  
Brain Cell ◽  
Mushroom Bodies ◽  
Brain Anatomy ◽  
Last Common Ancestor ◽  
Specific Expression ◽  
The Brain

Abstract Background The brain anatomy in the clade Spiralia can vary from simple, commissural brains (e.g., gastrotrichs, rotifers) to rather complex, partitioned structures (e.g., in cephalopods and annelids). How often and in which lineages complex brains evolved still remains unclear. Nemerteans are a clade of worm-like spiralians, which possess a complex central nervous system (CNS) with a prominent brain, and elaborated chemosensory and neuroglandular cerebral organs, which have been previously suggested as homologs to the annelid mushroom bodies. To understand the developmental and evolutionary origins of the complex brain in nemerteans and spiralians in general, we investigated details of the neuroanatomy and gene expression in the brain and cerebral organs of the juveniles of nemertean Lineus ruber. Results In the juveniles, the CNS is already composed of all major elements present in the adults, including the brain, paired longitudinal lateral nerve cords, and an unpaired dorsal nerve cord, which suggests that further neural development is mostly related with increase in the size but not in complexity. The ultrastructure of the juvenile cerebral organ revealed that it is composed of several distinct cell types present also in the adults. The 12 transcription factors commonly used as brain cell type markers in bilaterians show region-specific expression in the nemertean brain and divide the entire organ into several molecularly distinct areas, partially overlapping with the morphological compartments. Additionally, several of the mushroom body-specific genes are expressed in the developing cerebral organs. Conclusions The dissimilar expression of molecular brain markers between L. ruber and the annelid Platynereis dumerilii indicates that the complex brains present in those two species evolved convergently by independent expansions of non-homologous regions of a simpler brain present in their last common ancestor. Although the same genes are expressed in mushroom bodies and cerebral organs, their spatial expression within organs shows apparent differences between annelids and nemerteans, indicating convergent recruitment of the same genes into patterning of non-homologous organs or hint toward a more complicated evolutionary process, in which conserved and novel cell types contribute to the non-homologous structures.

scholarly journals Gene expression in the developing nemertean brain indicates convergent evolution of complex brains in Spiralia

2021 ◽  
Author(s):  
Ludwik Gąsiorowski ◽  
Aina Børve ◽  
Irina A. Cherneva ◽  
Andrea Orús-Alcalde ◽  
Andreas Hejnol
Keyword(s):  
Gene Expression ◽  
Neural Development ◽  
Cell Types ◽  
Major Elements ◽  
Mushroom Bodies ◽  
Animal Group ◽  
Evolutionary Origins ◽  
The Moment ◽  
Cerebral Organ ◽  
The Brain

AbstractBackgroundNemertea is a clade of worm-like animals, which belongs to a larger animal group called Spiralia (together with e.g. annelids, flatworms and mollusks). Many of the nemertean species possess a complex central nervous system (CNS) with a prominent brain, and elaborated chemosensory and neuroglandular cerebral organs, which have been suggested as homologues to the annelid mushroom bodies. In order to understand the developmental and evolutionary origins of complex nemertean brain, we investigated details of neuroanatomy and gene expression in the brain and cerebral organs of the juveniles of nemertean Lineus ruber.ResultsIn the hatched juveniles the CNS is already composed of all major elements present in the adults, including the brain (with dorsal and ventral lobes), paired longitudinal lateral nerve cords and an unpaired dorsal nerve cord. The TEM investigation of the juvenile cerebral organ revealed that the structure is already composed of several distinct cell types present also in the adults. We further investigated the expression of twelve transcription factors commonly used as brain and cell type markers in bilaterian brains, including genes specific for annelid mushroom bodies. The expression of the investigated genes in the brain is region-specific and divides the entire organ into several molecularly distinct areas, partially overlapping with the morphological compartments. Additionally, we detected expression of mushroom body specific genes in the developing cerebral organs.ConclusionsAt the moment of hatching, the juveniles of L. ruber already have a similar neuroarchitecture as adult worms, which suggests that further neural development is mostly related with increase in the size but not in complexity. Comparison in the gene expression between L. ruber and the annelid Platynereis dumerilii and other spiralians, indicates that the complex brains present in those two species evolved convergently by independent expansion of non-homologues regions of the simpler brain present in their common ancestor. The similarities in gene expression in mushroom bodies and cerebral organs might be a result of the convergent recruitment of the same genes into patterning of non-homologues organs or the results of more complicated evolutionary processes, in which conserved and novel cell types contribute to the non-homologues structures.

scholarly journals SARS-CoV-2 receptor and entry genes are expressed by sustentacular cells in the human olfactory neuroepithelium

2020 ◽  
Author(s):  
Leon Fodoulian ◽  
Joel Tuberosa ◽  
Daniel Rossier ◽  
Madlaina Boillat ◽  
Chenda Kan ◽  
...  
Keyword(s):  
Sensory System ◽  
Cell Types ◽  
Sensory Epithelium ◽  
Brain Cell ◽  
Rna Seq ◽  
Angiotensin Converting Enzyme 2 ◽  
Sustentacular Cells ◽  
The Brain ◽  
Brain Cell Types ◽  
Human And Mouse

AbstractVarious reports indicate an association between COVID-19 and anosmia, suggesting an infection of the olfactory sensory epithelium, and thus a possible direct virus access to the brain. To test this hypothesis, we generated RNA-seq libraries from human olfactory neuroepithelia, in which we found substantial expression of the genes coding for the virus receptor angiotensin-converting enzyme-2 (ACE2), and for the virus internalization enhancer TMPRSS2. We analyzed a human olfactory single-cell RNA-seq dataset and determined that sustentacular cells, which maintain the integrity of olfactory sensory neurons, express ACE2 and TMPRSS2. We then observed that the ACE2 protein was highly expressed in a subset of sustentacular cells in human and mouse olfactory tissues. Finally, we found ACE2 transcripts in specific brain cell types, both in mice and humans. Sustentacular cells thus represent a potential entry door for SARS-CoV-2 in a neuronal sensory system that is in direct connection with the brain.

scholarly journals Drosophila mef2 is essential for normal mushroom body and wing development

2018 ◽  
Author(s):  
Jill R. Crittenden ◽  
Efthimios M. C. Skoulakis ◽  
Elliott. S. Goldstein ◽  
Ronald L. Davis
Keyword(s):  
Nuclear Localization ◽  
Mushroom Body ◽  
Normal Development ◽  
Cell Types ◽  
Mushroom Bodies ◽  
Wing Development ◽  
Myocyte Enhancer Factor 2 ◽  
Multiple Cell ◽  
The Brain ◽  
Enhancer Factor

ABSTRACTMEF2 (myocyte enhancer factor 2) transcription factors are found in the brain and muscle of insects and vertebrates and are essential for the differentiation of multiple cell types. We show that in the fruitfly Drosophila, MEF2 is essential for normal development of wing veins, and for mushroom body formation in the brain. In embryos mutant for D-mef2, there was a striking reduction in the number of mushroom body neurons and their axon bundles were not detectable. D-MEF2 expression coincided with the formation of embryonic mushroom bodies and, in larvae, expression onset was confirmed to be in post-mitotic neurons. With a D-mef2 point mutation that disrupts nuclear localization, we find that D-MEF2 is restricted to a subset of Kenyon cells that project to the α/β, and γ axonal lobes of the mushroom bodies, but not to those forming the α’/β’ lobes. Our findings that ancestral mef2 is specifically important in dopamine-receptive neurons has broad implications for its function in mammalian neurocircuits.

scholarly journals Brain composition in Heliconius butterflies, post-eclosion growth and experience dependent neuropil plasticity

2015 ◽  
Author(s):  
Stephen H Montgomery ◽  
Richard M Merrill ◽  
Swidbert R Ott
Keyword(s):  
Behavioral Ecology ◽  
Neural Development ◽  
Mushroom Body ◽  
Brain Regions ◽  
Mushroom Bodies ◽  
Heliconius Butterflies ◽  
Sensory Adaptations ◽  
Differential Expansion ◽  
The Brain

Behavioral and sensory adaptations are often based in the differential expansion of brain components. These volumetric differences represent changes in investment, processing capacity and/or connectivity, and can be used to investigate functional and evolutionary relationships between different brain regions, and between brain composition and behavioral ecology. Here, we describe the brain composition of two species of Heliconius butterflies, a long-standing study system for investigating ecological adaptation and speciation. We confirm a previous report of striking mushroom body expansion, and explore patterns of post-eclosion growth and experience-dependent plasticity in neural development. This analysis uncovers age- and experience-dependent post-emergence mushroom body growth comparable to that in foraging hymenoptera, but also identifies plasticity in several other neuropil. An interspecific analysis indicates that Heliconius display remarkable levels of investment in mushroom bodies for a lepidopteran, and indeed rank highly compared to other insects. Our analyses lay the foundation for future comparative and experimental analyses that will establish Heliconius as a useful case study in evolutionary neurobiology.

scholarly journals Cell type-specific biotin labeling in vivo resolves regional neuronal proteomic differences in mouse brain

2021 ◽  
Author(s):  
Sruti Rayaprolu ◽  
Sara Bitarafan ◽  
Ranjita Betarbet ◽  
Sydney N Sunna ◽  
Lihong Cheng ◽  
...  
Keyword(s):  
Mouse Brain ◽  
Neurological Diseases ◽  
Neuronal Cell ◽  
Cell Types ◽  
Proteomic Profiling ◽  
Cell Type ◽  
Specific Expression ◽  
Cell Type Specific ◽  
The Brain

Isolation and proteomic profiling of brain cell types, particularly neurons, pose several technical challenges which limit our ability to resolve distinct cellular phenotypes in neurological diseases. Therefore, we generated a novel mouse line that enables cell type-specific expression of a biotin ligase, TurboID, via Cre-lox strategy for in vivo proximity-dependent biotinylation of proteins. Using adenoviral-based and transgenic approaches, we show striking protein biotinylation in neuronal cell bodies and axons throughout the mouse brain. We quantified more than 2,000 neuron-derived proteins following enrichment that mapped to numerous subcellular compartments. Synaptic, transmembrane transporters, ion channel subunits, and disease-relevant druggable targets were among the most significantly enriched proteins. Remarkably, we resolved brain region-specific proteomic profiles of Camk2a neurons with distinct functional molecular signatures and disease associations that may underlie regional neuronal vulnerability. Leveraging the neuronal specificity of this in vivo biotinylation strategy, we used an antibody-based approach to uncover regionally unique patterns of neuron-derived signaling phospho-proteins and cytokines, particularly in the cortex and cerebellum. Our work provides a proteomic framework to investigate cell type-specific mechanisms driving physiological and pathological states of the brain as well as complex tissues beyond the brain.

scholarly journals A Cluster of Four Surface Antigen Genes Specifically Expressed in Bradyzoites, SAG2CDXY, Plays an Important Role in Toxoplasma gondii Persistence

2008 ◽  
Vol 76 (6) ◽  
pp. 2402-2410 ◽  
Author(s):  
Jeroen P. J. Saeij ◽  
Gustavo Arrizabalaga ◽  
John C. Boothroyd
Keyword(s):  
Toxoplasma Gondii ◽  
Surface Antigen ◽  
Chronic Infection ◽  
Cell Types ◽  
Firefly Luciferase ◽  
Specific Expression ◽  
Genes Encoding ◽  
Tandem Genes ◽  
Different Cell Types ◽  
The Brain

ABSTRACT Toxoplasma gondii is one of the most successful protozoan parasites of warm-blooded animals. Stage-specific expression of its surface molecules is thought to be key to its ability to establish chronic infection in immunocompetent animals. The rapidly dividing tachyzoite stage displays a different subset of family of surface antigen 1 (SAG1)-related sequences (SRSs) from that displayed by the encysted bradyzoite stage. It is possible that this switch is necessary to protect the bradyzoites against an immune response raised against the tachyzoite stage. Alternatively, it might be that bradyzoite SRSs evolved to facilitate invasion of different cell types, such as those found in the brain, where cysts develop, or the small intestine, where bradyzoites must enter after oral infection. Here we studied the function of a cluster of four tandem genes, encoding bradyzoite SRSs called SAG2C, -D, -X, and -Y. Using bioluminescence imaging of mice infected with parasites expressing firefly luciferase (FLUC) driven by the SAG2D promoter, we show stage conversion for the first time in living animals. A truncated version of the SAG2D promoter (SAG2Dmin) gave efficient expression of FLUC in both tachyzoites and bradyzoites, indicating that the bradyzoite specificity of the complete SAG2D promoter is likely due to an element(s) that normally suppresses expression in tachyzoites. Comparing mice infected with the wild type or a mutant where the SAG2CDXY cluster of genes has been deleted (ΔSAG2CDXY), we demonstrate that whereas ΔSAG2CDXY parasites are less capable of maintaining a chronic infection in the brain, they do not show a defect in oral infectivity.

scholarly journals Cell-Type Specific Analysis of Selenium-Related Genes in Brain

Antioxidants ◽  
2019 ◽  
Vol 8 (5) ◽  
pp. 120
Author(s):  
Alexandru R. Sasuclark ◽  
Vedbar S. Khadka ◽  
Matthew W. Pitts
Keyword(s):  
Neural Development ◽  
Cortical Neurons ◽  
Cell Types ◽  
Inhibitory Neurons ◽  
Brain Atlas ◽  
Cell Type ◽  
Specific Expression ◽  
Rnaseq Data ◽  
Cell Type Specific Expression ◽  
Cell Type Specific

Selenoproteins are a unique class of proteins that play key roles in redox signaling in the brain. This unique organ is comprised of a wide variety of cell types that includes excitatory neurons, inhibitory neurons, astrocytes, microglia, and oligodendrocytes. Whereas selenoproteins are known to be required for neural development and function, the cell-type specific expression of selenoproteins and selenium-related machinery has yet to be systematically investigated. Due to advances in sequencing technology and investment from the National Institutes of Health (NIH)-sponsored BRAIN initiative, RNA sequencing (RNAseq) data from thousands of cortical neurons can now be freely accessed and searched using the online RNAseq data navigator at the Allen Brain Atlas. Hence, we utilized this newly developed tool to perform a comprehensive analysis of the cell-type specific expression of selenium-related genes in brain. Select proteins of interest were further verified by means of multi-label immunofluorescent labeling of mouse brain sections. Of potential significance to neural selenium homeostasis, we report co-expression of selenoprotein P (SELENOP) and selenium binding protein 1 (SELENBP1) within astrocytes. These findings raise the intriguing possibility that SELENBP1 may negatively regulate astrocytic SELENOP synthesis and thereby limit downstream Se supply to neurons.

Similarities and differences in the subcellular localization of hamartin and tuberin in the kidney

2000 ◽  
Vol 278 (5) ◽  
pp. F737-F746 ◽  
Author(s):  
Vanishree Murthy ◽  
Luciana A. Haddad ◽  
Nicole Smith ◽  
Denise Pinney ◽  
Robert Tyszkowski ◽  
...  
Keyword(s):  
Apical Membrane ◽  
Cell Types ◽  
Intercalated Cells ◽  
Autosomal Dominant Disorder ◽  
Specific Expression ◽  
Multiple Organs ◽  
Distal Tubules ◽  
Kidney Lesions ◽  
The Brain

Tuberous sclerosis complex (TSC) is an autosomal dominant disorder characterized by hamartomas in multiple organs, notably the brain and kidneys. The disease is caused by mutations in TSC1or TSC2 genes, coding hamartin and tuberin, respectively. Immunofluorescence analysis of tuberin and hamartin performed here demonstrates that both proteins are specifically expressed in the distal urinary tubule, comprising the distal tubules, connecting segment, and collecting ducts. Hamartin, distinct from tuberin, is expressed in the thick ascending limbs of Henle and in juxtaglomerular cells, where it colocalizes with renin. In positive epithelial cells, tuberin localizes to the cytoplasm as well as the apical membrane. Hamartin, however, preferentially localizes to the apical membrane. The two proteins colocalize at the apical membrane of type A intercalated cells and connecting tubule cells, whereas in type B intercalated cells they reveal a variable pattern of expression. The cell-specific expression of tuberin and hamartin described here will provide critical insight into the cell types that give rise to kidney lesions, and the tumor suppressor role of these proteins in TSC.

scholarly journals Brain Microenvironment Heterogeneity: Potential Value for Brain Tumors

2021 ◽  
Vol 11 ◽  
Author(s):  
Laura Álvaro-Espinosa ◽  
Ana de Pablos-Aragoneses ◽  
Manuel Valiente ◽  
Neibla Priego
Keyword(s):  
Brain Tumors ◽  
Single Cell ◽  
Brain Injuries ◽  
Clinical Work ◽  
Cell Types ◽  
Brain Cell ◽  
Brain Disorders ◽  
Brain Connectome ◽  
The Brain ◽  
Brain Cell Types

Uncovering the complexity of the microenvironment that emerges in brain disorders is key to identify potential vulnerabilities that might help challenging diseases affecting this organ. Recently, genomic and proteomic analyses, especially at the single cell level, have reported previously unrecognized diversity within brain cell types. The complexity of the brain microenvironment increases during disease partly due to the immune infiltration from the periphery that contributes to redefine the brain connectome by establishing a new crosstalk with resident brain cell types. Within the rewired brain ecosystem, glial cell subpopulations are emerging hubs modulating the dialogue between the Immune System and the Central Nervous System with important consequences in the progression of brain tumors and other disorders. Single cell technologies are crucial not only to define and track the origin of disease-associated cell types, but also to identify their molecular similarities and differences that might be linked to specific brain injuries. These altered molecular patterns derived from reprogramming the healthy brain into an injured organ, might provide a new generation of therapeutic targets to challenge highly prevalent and lethal brain disorders that remain incurable with unprecedented specificity and limited toxicities. In this perspective, we present the most relevant clinical and pre-clinical work regarding the characterization of the heterogeneity within different components of the microenvironment in the healthy and injured brain with a special interest on single cell analysis. Finally, we discuss how understanding the diversity of the brain microenvironment could be exploited for translational purposes, particularly in primary and secondary tumors affecting the brain.

scholarly journals Early-life nutrition interacts with developmental genes to shape the brain and sleep behavior in Drosophila melanogaster

2020 ◽  
Author(s):  
Gonzalo H. Olivares ◽  
Franco Núñez ◽  
Noemi Candia ◽  
Karen Oróstica ◽  
Franco Vega-Macaya ◽  
...  
Keyword(s):  
Genetic Variation ◽  
Neural Development ◽  
Insulin Signaling ◽  
Early Life ◽  
Natural Variation ◽  
Mushroom Bodies ◽  
Variable Response ◽  
Sleep Behavior ◽  
Nutritional Environment ◽  
The Brain

AbstractThe genetic variation of complex behaviors depends on the variation of brain structure and organization. The mechanisms by which the genome interacts with the nutritional environment during development to shape the brain and behaviors of adults are not well understood. Here we use the Drosophila Genetic Reference Panel to identify genes and pathways underlying this interaction in sleep behavior and mushroom bodies morphology.We identify genes associated with sleep sensitivity to early nutrition, from which protein networks responsible for translation, endocytosis regulation, ubiquitination, lipid metabolism, and neural development emerge. We confirm that genes regulating neural development and insulin signaling in mushroom bodies contribute to the variable response to nutrition. We propose that natural variation in genes that control the development of the brain interact with early-life malnutrition to contribute to variation of adult sleep behavior.

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