Transcriptome Analysis of NPFR Neurons Reveals a Connection Between proteome Diversity and Social Behavior

AbstractComplex social behaviors are mediated by the activity of highly intricate neuronal networks, the function of which is shaped by their transcriptomic and proteomic content. Contemporary advances in neurogenetics, genomics, and tools for automated behavior analysis make it possible to functionally connect the transcriptome profile of candidate neurons to their role in regulating behavior. In this study we used Drosophila melanogaster to explore the molecular signature of neurons expressing receptor for neuropeptide F (NPF), the fly homologue of neuropeptide Y (NPY). By comparing the transcription profile of NPFR neurons to those of nine other populations of neurons, we discovered that NPFR neurons exhibit a unique transcriptome, enriched with receptors for various neuropeptides and neuromodulators, as well as with genes known to regulate behavioral processes, such as learning and memory. By manipulating RNA editing and protein ubiquitination programs specifically in NPFR neurons, we demonstrate that their delicate transcriptome and proteome repertoires are required to suppress male courtship and certain features of social group interaction. Our results highlight the importance of transcriptome and proteome diversity in the regulation of complex behaviors and pave the path for future dissection of the spatiotemporal regulation of genes within highly complex tissues, such as the brain.

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Transcriptome Analysis of NPFR Neurons Reveals a Connection Between Proteome Diversity and Social Behavior

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2021.628662 ◽

2021 ◽

Vol 15 ◽

Author(s):

Julia Ryvkin ◽

Assa Bentzur ◽

Anat Shmueli ◽

Miriam Tannenbaum ◽

Omri Shallom ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Social Behavior ◽

Transcriptome Analysis ◽

Molecular Signature ◽

Transcription Profile ◽

Male Courtship ◽

Transcriptome Profile ◽

Protein Ubiquitination ◽

Spatiotemporal Regulation ◽

The Brain

Social behaviors are mediated by the activity of highly complex neuronal networks, the function of which is shaped by their transcriptomic and proteomic content. Contemporary advances in neurogenetics, genomics, and tools for automated behavior analysis make it possible to functionally connect the transcriptome profile of candidate neurons to their role in regulating behavior. In this study we used Drosophila melanogaster to explore the molecular signature of neurons expressing receptor for neuropeptide F (NPF), the fly homolog of neuropeptide Y (NPY). By comparing the transcription profile of NPFR neurons to those of nine other populations of neurons, we discovered that NPFR neurons exhibit a unique transcriptome, enriched with receptors for various neuropeptides and neuromodulators, as well as with genes known to regulate behavioral processes, such as learning and memory. By manipulating RNA editing and protein ubiquitination programs specifically in NPFR neurons, we demonstrate that the proper expression of their unique transcriptome and proteome is required to suppress male courtship and certain features of social group interaction. Our results highlight the importance of transcriptome and proteome diversity in the regulation of complex behaviors and pave the path for future dissection of the spatiotemporal regulation of genes within highly complex tissues, such as the brain.

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IDENTIFICATION OF BRAIN SITES CONTROLLING FEMALE RECEPTIVITY IN MOSAICS OF DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/103.2.179 ◽

1983 ◽

Vol 103 (2) ◽

pp. 179-195

Author(s):

Laurie Tompkins ◽

Jeffrey C Hall

Keyword(s):

Drosophila Melanogaster ◽

Minimum Amount ◽

Male Courtship ◽

Experimental Conditions ◽

Female Receptivity ◽

Female Genotype ◽

Courtship Behaviors ◽

Necessary And Sufficient ◽

The Brain ◽

Male Genotype

ABSTRACT We have identified cells in the brain of Drosophila melanogaster that are required to be of female genotype for receptivity to copulation with males. To do this, we determined experimental conditions in which female flies virtually always copulate, then measured the minimum amount of male courtship that is required to stimulate females to indicate their receptivity to copulation. We then observed gynandromorphs with female genitalia to determine whether the sex mosaics elicited at least the minimum amount of courtship and, if so, whether they copulated. By analyzing these gynandromorphs, in which the genotype of external and internal tissues could be ascertained, we were able to identify a group of cells in the dorsal anterior brain that, when bilaterally female, is necessary and sufficient for receptivity to copulation. This group of cells is anatomically distinct from those that are required to be of male genotype for the performance of courtship behaviors.

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Effets de deux mutations neurologiques, minibrain3 et no-bridgeKS49, sur la parade nuptiale chez Drosophila melanogaster

Canadian Journal of Zoology ◽

10.1139/z93-130 ◽

1993 ◽

Vol 71 (5) ◽

pp. 985-990 ◽

Cited By ~ 1

Author(s):

A. Bouhouche ◽

T. Benziane ◽

G. Vaysse

Keyword(s):

Drosophila Melanogaster ◽

Sequential Analysis ◽

Low Frequency ◽

Male Courtship ◽

Protocerebral Bridge ◽

Copulation Attempt ◽

The Brain

Male courtship events of two neurological mutants (nobridgeKS49 (nob) and minibrain3 (mnb)) of Drosophila melanogaster were recorded and subjected to quantitative and sequential analysis. The nob mutation, which disorganizes the protocerebral bridge, causes specific defects in courtship: a low frequency of the copulation attempt and the disappearance of the licking – copulation attempt sequence. Thus, the nob males were unable to copulate with receptive females within the 30-min observation. We think that this may be due to an abnormality in their wing vibrations. The mnb mutant, characterized by a reduction of the brain (by more than 50%), exhibited difficulties in initiating courtship and in maintaining contact with the female during courtship. These courtship defects may be due to visual and locomotor anomalies.

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233 ASSOCIATION OF THE BOVINE 2-CELL-STAGE BLASTOMERE TRANSCRIPTOME PROFILE WITH THE INDIVIDUAL DEVELOPMENTAL POTENTIAL OF THE SISTER BLASTOMERE

Reproduction Fertility and Development ◽

10.1071/rdv25n1ab233 ◽

2013 ◽

Vol 25 (1) ◽

pp. 264

Author(s):

E. Held ◽

D. Salilew-Wondim ◽

D. Tesfaye ◽

K. Schellander ◽

M. Hoelker

Keyword(s):

Transcriptome Analysis ◽

Molecular Mechanisms ◽

Early Stage ◽

Transcriptome Profiling ◽

Microarray Platform ◽

Developmental Competence ◽

Transcriptome Profile ◽

Cell Stage ◽

Developmental Potential ◽

Protein Ubiquitination

Transcriptome profiling has been used to identify genes related to developmental competence in bovine embryos and oocytes for several years. However, the direct relationship between the transcriptome profile and developmental potential of the same pre-implantation embryo is missing. Therefore, in the present study, one blastomere of a 2-cell-stage embryo was taken as a biopsy and immediately snap-frozen for transcriptome analysis; the sister blastomere was cultured individually in a well-of-the-well culture system. Frozen individual blastomeres taking the form of 2-cell-stage embryos were pooled together, depending on the developmental destination of the sister blastomeres. Accordingly, three groups were defined: 1) embryos that did not cleave after separation (2CB), 2) embryos arrested before embryonic genome activation (8CB), and 3) embryos that reached the blastocyst stage (BL). On the basis of these developmental phenotypes, blastomeres were pooled and used for transcriptome analysis, using a bovine EmbryoGene microarray platform (Agilent Technologies, Santa Clara, CA, USA). Results revealed 632 genes to be differentially regulated (fold change, P ≥ 1.5, P ≤ 0.05; FDR, P ≤ 0.1) between competent (BL group) and incompetent 2-cell-stage embryos (2CB) as well as 150 genes between the BL group and 8CB. Seventy-seven genes were commonly differentially regulated. Functional annotation analyses of differentially regulated genes indicated those genes to be involved in the protein ubiquitination pathway on the one hand and in the oxidative stress response, including oxidoreductase, peroxidase, and antioxidant activity, as well in oxidative phosphorylation (e.g. NDUFS1, MAPK14, CAT, PRDX1, and PRDX6) on the other hand. Furthermore, selected candidate genes known to function as direct and indirect scavengers of reactive oxygen species (ROS) were analysed for their expression in an independent model for developmental competence; namely, early- and late-cleaved 2-cell-stage embryos. Moreover, ROS detection was performed, showing higher accumulation of ROS in late-cleaved 2-cell-stage embryos, whereas lower ROS levels were detected in early-cleaved 2-cell-stage embryos associated with higher expression of ROS scavengers. The overall findings of the present study indicate the potential of using blastomere biopsies at 2-cell-stage embryos for molecular analysis to understand the molecular mechanisms associated with the further developmental competence of early-stage embryos.

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