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  1. Article ; Online: Mapping of multiple neurotransmitter receptor subtypes and distinct protein complexes to the connectome.

    Sanfilippo, Piero / Kim, Alexander J / Bhukel, Anuradha / Yoo, Juyoun / Mirshahidi, Pegah S / Pandey, Vijaya / Bevir, Harry / Yuen, Ashley / Mirshahidi, Parmis S / Guo, Peiyi / Li, Hong-Sheng / Wohlschlegel, James A / Aso, Yoshinori / Zipursky, S Lawrence

    Neuron

    2024  Volume 112, Issue 6, Page(s) 942–958.e13

    Abstract: Neurons express various combinations of neurotransmitter receptor (NR) subunits and receive inputs from multiple neuron types expressing different neurotransmitters. Localizing NR subunits to specific synaptic inputs has been challenging. Here, we use ... ...

    Abstract Neurons express various combinations of neurotransmitter receptor (NR) subunits and receive inputs from multiple neuron types expressing different neurotransmitters. Localizing NR subunits to specific synaptic inputs has been challenging. Here, we use epitope-tagged endogenous NR subunits, expansion light-sheet microscopy, and electron microscopy (EM) connectomics to molecularly characterize synapses in Drosophila. We show that in directionally selective motion-sensitive neurons, different multiple NRs elaborated a highly stereotyped molecular topography with NR localized to specific domains receiving cell-type-specific inputs. Developmental studies suggested that NRs or complexes of them with other membrane proteins determine patterns of synaptic inputs. In support of this model, we identify a transmembrane protein selectively associated with a subset of spatially restricted synapses and demonstrate its requirement for synapse formation through genetic analysis. We propose that mechanisms that regulate the precise spatial distribution of NRs provide a molecular cartography specifying the patterns of synaptic connections onto dendrites.
    MeSH term(s) Connectome ; Synapses/physiology ; Motor Neurons/metabolism ; Microscopy, Electron ; Receptors, GABA-A/metabolism
    Chemical Substances Receptors, GABA-A
    Language English
    Publishing date 2024-01-22
    Publishing country United States
    Document type Journal Article
    ZDB-ID 808167-0
    ISSN 1097-4199 ; 0896-6273
    ISSN (online) 1097-4199
    ISSN 0896-6273
    DOI 10.1016/j.neuron.2023.12.014
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  2. Article: Landscape and evolution of tissue-specific alternative polyadenylation across Drosophila species

    Sanfilippo, Piero / Lai, Eric C / Wen, Jiayu

    Genome biology. 2017 Dec., v. 18, no. 1

    2017  

    Abstract: BACKGROUND: Drosophila melanogaster has one of best-described transcriptomes of any multicellular organism. Nevertheless, the paucity of 3′-sequencing data in this species precludes comprehensive assessment of alternative polyadenylation (APA), which is ... ...

    Abstract BACKGROUND: Drosophila melanogaster has one of best-described transcriptomes of any multicellular organism. Nevertheless, the paucity of 3′-sequencing data in this species precludes comprehensive assessment of alternative polyadenylation (APA), which is subject to broad tissue-specific control. RESULTS: Here, we generate deep 3′-sequencing data from 23 developmental stages, tissues, and cell lines of D. melanogaster, yielding a comprehensive atlas of ~ 62,000 polyadenylated ends. These data broadly extend the annotated transcriptome, identify ~ 40,000 novel 3′ termini, and reveal that two-thirds of Drosophila genes are subject to APA. Furthermore, we dramatically expand the numbers of genes known to be subject to tissue-specific APA, such as 3′ untranslated region (UTR) lengthening in head and 3′ UTR shortening in testis, and characterize new tissue and developmental 3′ UTR patterns. Our thorough 3′ UTR annotations permit reassessment of post-transcriptional regulatory networks, via conserved miRNA and RNA binding protein sites. To evaluate the evolutionary conservation and divergence of APA patterns, we generate developmental and tissue-specific 3′-seq libraries from Drosophila yakuba and Drosophila virilis. We document broadly analogous tissue-specific APA trends in these species, but also observe significant alterations in 3′ end usage across orthologs. We exploit the population of functionally evolving poly(A) sites to gain clear evidence that evolutionary divergence in core polyadenylation signal (PAS) and downstream sequence element (DSE) motifs drive broad alterations in 3′ UTR isoform expression across the Drosophila phylogeny. CONCLUSIONS: These data provide a critical resource for the Drosophila community and offer many insights into the complex control of alternative tissue-specific 3′ UTR formation and its consequences for post-transcriptional regulatory networks.
    Keywords cell lines ; developmental stages ; divergent evolution ; Drosophila melanogaster ; Drosophila virilis ; Drosophila yakuba ; genes ; head ; microRNA ; phylogeny ; RNA-binding proteins ; testes ; transcriptome
    Language English
    Dates of publication 2017-12
    Size p. 229.
    Publishing place BioMed Central
    Document type Article
    ZDB-ID 2040529-7
    ISSN 1474-760X ; 1465-6914 ; 1465-6906
    ISSN (online) 1474-760X ; 1465-6914
    ISSN 1465-6906
    DOI 10.1186/s13059-017-1358-0
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  3. Article: Genome-wide profiling of the 3' ends of polyadenylated RNAs

    Sanfilippo, Piero / Eric C. Lai / Pedro Miura

    Methods. 2017 Aug. 15, v. 126

    2017  

    Abstract: Alternative polyadenylation (APA) diversifies the 3′ termini of a majority of mRNAs in most eukaryotes, and is consequently inferred to have substantial consequences for the utilization of post-transcriptional regulatory mechanisms. Since conventional ... ...

    Abstract Alternative polyadenylation (APA) diversifies the 3′ termini of a majority of mRNAs in most eukaryotes, and is consequently inferred to have substantial consequences for the utilization of post-transcriptional regulatory mechanisms. Since conventional RNA-sequencing methods do not accurately define mRNA termini, a number of protocols have been developed that permit sequencing of the 3′ ends of polyadenylated transcripts (3′-seq). We present here our experimental protocol to generate 3′-seq libraries using a dT-priming approach, including extensive details on considerations that will enable successful library cloning. We pair this with a set of computational tools that allow the user to process the raw sequence data into a filtered set of clusters that represent high-confidence functional polyadenylation sites. The data are single-nucleotide resolution and quantitative, and can be used for downstream analyses of APA.
    Keywords 3' untranslated regions ; DNA libraries ; eukaryotic cells ; sequence analysis
    Language English
    Dates of publication 2017-0815
    Size p. 86-94.
    Publishing place Elsevier Inc.
    Document type Article
    ZDB-ID 1066584-5
    ISSN 1095-9130 ; 1046-2023
    ISSN (online) 1095-9130
    ISSN 1046-2023
    DOI 10.1016/j.ymeth.2017.06.003
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  4. Article ; Online: Landscape and evolution of tissue-specific alternative polyadenylation across Drosophila species.

    Sanfilippo, Piero / Wen, Jiayu / Lai, Eric C

    Genome biology

    2017  Volume 18, Issue 1, Page(s) 229

    Abstract: Background: Drosophila melanogaster has one of best-described transcriptomes of any multicellular organism. Nevertheless, the paucity of 3'-sequencing data in this species precludes comprehensive assessment of alternative polyadenylation (APA), which is ...

    Abstract Background: Drosophila melanogaster has one of best-described transcriptomes of any multicellular organism. Nevertheless, the paucity of 3'-sequencing data in this species precludes comprehensive assessment of alternative polyadenylation (APA), which is subject to broad tissue-specific control.
    Results: Here, we generate deep 3'-sequencing data from 23 developmental stages, tissues, and cell lines of D. melanogaster, yielding a comprehensive atlas of ~ 62,000 polyadenylated ends. These data broadly extend the annotated transcriptome, identify ~ 40,000 novel 3' termini, and reveal that two-thirds of Drosophila genes are subject to APA. Furthermore, we dramatically expand the numbers of genes known to be subject to tissue-specific APA, such as 3' untranslated region (UTR) lengthening in head and 3' UTR shortening in testis, and characterize new tissue and developmental 3' UTR patterns. Our thorough 3' UTR annotations permit reassessment of post-transcriptional regulatory networks, via conserved miRNA and RNA binding protein sites. To evaluate the evolutionary conservation and divergence of APA patterns, we generate developmental and tissue-specific 3'-seq libraries from Drosophila yakuba and Drosophila virilis. We document broadly analogous tissue-specific APA trends in these species, but also observe significant alterations in 3' end usage across orthologs. We exploit the population of functionally evolving poly(A) sites to gain clear evidence that evolutionary divergence in core polyadenylation signal (PAS) and downstream sequence element (DSE) motifs drive broad alterations in 3' UTR isoform expression across the Drosophila phylogeny.
    Conclusions: These data provide a critical resource for the Drosophila community and offer many insights into the complex control of alternative tissue-specific 3' UTR formation and its consequences for post-transcriptional regulatory networks.
    MeSH term(s) 3' Untranslated Regions ; Animals ; Cell Line ; Computational Biology/methods ; Drosophila/embryology ; Drosophila/genetics ; Drosophila melanogaster/genetics ; Evolution, Molecular ; Molecular Sequence Annotation ; Organ Specificity/genetics ; Poly A ; Polyadenylation ; RNA Isoforms ; RNA-Binding Proteins/metabolism ; Species Specificity ; Transcription, Genetic
    Chemical Substances 3' Untranslated Regions ; RNA Isoforms ; RNA-Binding Proteins ; Poly A (24937-83-5)
    Language English
    Publishing date 2017-11-30
    Publishing country England
    Document type Journal Article
    ZDB-ID 2040529-7
    ISSN 1474-760X ; 1474-760X
    ISSN (online) 1474-760X
    ISSN 1474-760X
    DOI 10.1186/s13059-017-1358-0
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  5. Article: Constitutive and conditional epitope-tagging of endogenous G protein coupled receptors in

    Bonanno, Shivan L / Sanfilippo, Piero / Eamani, Aditya / Sampson, Maureen M / Binu, Kandagedon / Li, Kenneth / Burns, Giselle D / Makar, Marylyn E / Zipursky, S Lawrence / Krantz, David E

    bioRxiv : the preprint server for biology

    2023  

    Abstract: To visualize the cellular and subcellular localization of neuromodulatory G-protein coupled receptors (GPCRs) in : Significance statement: ... ...

    Abstract To visualize the cellular and subcellular localization of neuromodulatory G-protein coupled receptors (GPCRs) in
    Significance statement: In
    Language English
    Publishing date 2023-12-27
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2023.12.27.573472
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  6. Article: Mapping of multiple neurotransmitter receptor subtypes and distinct protein complexes to the connectome.

    Sanfilippo, Piero / Kim, Alexander J / Bhukel, Anuradha / Yoo, Juyoun / Mirshahidi, Pegah S / Pandey, Vijaya / Bevir, Harry / Yuen, Ashley / Mirshahidi, Parmis S / Guo, Peiyi / Li, Hong-Sheng / Wohlschlegel, James A / Aso, Yoshinori / Zipursky, S Lawrence

    bioRxiv : the preprint server for biology

    2023  

    Abstract: Neurons express different combinations of neurotransmitter receptor (NR) subunits and receive inputs from multiple neuron types expressing different neurotransmitters. Localizing NR subunits to specific synaptic inputs has been challenging. Here we use ... ...

    Abstract Neurons express different combinations of neurotransmitter receptor (NR) subunits and receive inputs from multiple neuron types expressing different neurotransmitters. Localizing NR subunits to specific synaptic inputs has been challenging. Here we use epitope tagged endogenous NR subunits, expansion light-sheet microscopy, and EM connectomics to molecularly characterize synapses in Drosophila. We show that in directionally selective motion sensitive neurons, different multiple NRs elaborated a highly stereotyped molecular topography with NR localized to specific domains receiving cell-type specific inputs. Developmental studies suggested that NRs or complexes of them with other membrane proteins determines patterns of synaptic inputs. In support of this model, we identify a transmembrane protein associated selectively with a subset of spatially restricted synapses and demonstrate through genetic analysis its requirement for synapse formation. We propose that mechanisms which regulate the precise spatial distribution of NRs provide a molecular cartography specifying the patterns of synaptic connections onto dendrites.
    Language English
    Publishing date 2023-10-02
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2023.10.02.560011
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  7. Article ; Online: Genome-wide profiling of the 3' ends of polyadenylated RNAs.

    Sanfilippo, Piero / Miura, Pedro / Lai, Eric C

    Methods (San Diego, Calif.)

    2017  Volume 126, Page(s) 86–94

    Abstract: Alternative polyadenylation (APA) diversifies the 3' termini of a majority of mRNAs in most eukaryotes, and is consequently inferred to have substantial consequences for the utilization of post-transcriptional regulatory mechanisms. Since conventional ... ...

    Abstract Alternative polyadenylation (APA) diversifies the 3' termini of a majority of mRNAs in most eukaryotes, and is consequently inferred to have substantial consequences for the utilization of post-transcriptional regulatory mechanisms. Since conventional RNA-sequencing methods do not accurately define mRNA termini, a number of protocols have been developed that permit sequencing of the 3' ends of polyadenylated transcripts (3'-seq). We present here our experimental protocol to generate 3'-seq libraries using a dT-priming approach, including extensive details on considerations that will enable successful library cloning. We pair this with a set of computational tools that allow the user to process the raw sequence data into a filtered set of clusters that represent high-confidence functional polyadenylation sites. The data are single-nucleotide resolution and quantitative, and can be used for downstream analyses of APA.
    MeSH term(s) 3' Untranslated Regions/physiology ; Animals ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Drosophila melanogaster ; Gene Expression Profiling/methods ; Genome-Wide Association Study/methods ; RNA, Messenger/genetics ; RNA, Messenger/metabolism
    Chemical Substances 3' Untranslated Regions ; Drosophila Proteins ; RNA, Messenger
    Language English
    Publishing date 2017-06-08
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 1066584-5
    ISSN 1095-9130 ; 1046-2023
    ISSN (online) 1095-9130
    ISSN 1046-2023
    DOI 10.1016/j.ymeth.2017.06.003
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  8. Article ; Online: Transcriptional Programs of Circuit Assembly in the Drosophila Visual System.

    Kurmangaliyev, Yerbol Z / Yoo, Juyoun / Valdes-Aleman, Javier / Sanfilippo, Piero / Zipursky, S Lawrence

    Neuron

    2020  Volume 108, Issue 6, Page(s) 1045–1057.e6

    Abstract: Precise patterns of synaptic connections between neurons are encoded in their genetic programs. Here, we use single-cell RNA sequencing to profile neuronal transcriptomes at multiple stages in the developing Drosophila visual system. We devise an ... ...

    Abstract Precise patterns of synaptic connections between neurons are encoded in their genetic programs. Here, we use single-cell RNA sequencing to profile neuronal transcriptomes at multiple stages in the developing Drosophila visual system. We devise an efficient strategy for profiling neurons at multiple time points in a single pool, thereby minimizing batch effects and maximizing the reliability of time-course data. A transcriptional atlas spanning multiple stages is generated, including more than 150 distinct neuronal populations; of these, 88 are followed through synaptogenesis. This analysis reveals a common (pan-neuronal) program unfolding in highly coordinated fashion in all neurons, including genes encoding proteins comprising the core synaptic machinery and membrane excitability. This program is overlaid by cell-type-specific programs with diverse cell recognition molecules expressed in different combinations and at different times. We propose that a pan-neuronal program endows neurons with the competence to form synapses and that cell-type-specific programs control synaptic specificity.
    MeSH term(s) Animals ; Axons/physiology ; Drosophila/physiology ; Neurogenesis/physiology ; Neurons/physiology ; Synapses/physiology ; Transcriptome ; Visual Pathways/physiology
    Language English
    Publishing date 2020-10-29
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 808167-0
    ISSN 1097-4199 ; 0896-6273
    ISSN (online) 1097-4199
    ISSN 0896-6273
    DOI 10.1016/j.neuron.2020.10.006
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  9. Article ; Online: Synaptic gradients transform object location to action.

    Dombrovski, Mark / Peek, Martin Y / Park, Jin-Yong / Vaccari, Andrea / Sumathipala, Marissa / Morrow, Carmen / Breads, Patrick / Zhao, Arthur / Kurmangaliyev, Yerbol Z / Sanfilippo, Piero / Rehan, Aadil / Polsky, Jason / Alghailani, Shada / Tenshaw, Emily / Namiki, Shigehiro / Zipursky, S Lawrence / Card, Gwyneth M

    Nature

    2023  Volume 613, Issue 7944, Page(s) 534–542

    Abstract: To survive, animals must convert sensory information into appropriate ... ...

    Abstract To survive, animals must convert sensory information into appropriate behaviours
    MeSH term(s) Animals ; Brain/cytology ; Brain/physiology ; Drosophila/anatomy & histology ; Drosophila/cytology ; Drosophila/physiology ; Neurons/physiology ; Visual Fields/physiology ; Synapses/metabolism ; Behavior, Animal ; Axons ; Psychomotor Performance ; Dendrites ; Escape Reaction
    Language English
    Publishing date 2023-01-04
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 120714-3
    ISSN 1476-4687 ; 0028-0836
    ISSN (online) 1476-4687
    ISSN 0028-0836
    DOI 10.1038/s41586-022-05562-8
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  10. Article ; Online: Publisher Correction: Synaptic gradients transform object location to action.

    Dombrovski, Mark / Peek, Martin Y / Park, Jin-Yong / Vaccari, Andrea / Sumathipala, Marissa / Morrow, Carmen / Breads, Patrick / Zhao, Arthur / Kurmangaliyev, Yerbol Z / Sanfilippo, Piero / Rehan, Aadil / Polsky, Jason / Alghailani, Shada / Tenshaw, Emily / Namiki, Shigehiro / Zipursky, S Lawrence / Card, Gwyneth M

    Nature

    2023  Volume 615, Issue 7954, Page(s) E26

    Language English
    Publishing date 2023-03-13
    Publishing country England
    Document type Published Erratum
    ZDB-ID 120714-3
    ISSN 1476-4687 ; 0028-0836
    ISSN (online) 1476-4687
    ISSN 0028-0836
    DOI 10.1038/s41586-023-05930-y
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