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Robert Carrillo

TitleAssociate Professor
InstitutionUniversity of Chicago
DepartmentMolecular Genetics and Cell Biology
AddressChicago IL 60637
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    Collapse Overview 
    Collapse overview
    The long term goals of my lab are to understand the molecules and developmental programs that regulate neuronal development and wiring. To this end, we investigated the novel interactions between two subfamilies of the immunoglobulin superfamily in Drosophila melanogaster (in collaboration with Christopher Garcia at Stanford and Engin Ozkan at the University of Chicago; Ozkan et al., 2013): the 21-member Dprs and the 9-member DIPs. Previously, we found that an interacting Dpr-DIP pair functions at various developmental stages including motor neuron development at the larval neuromuscular junction (NMJ) and wiring and cell survival in the pupal optic lobe (Carrillo et al., 2015). In my lab, we will explore the functions of cell surface proteins, including Dprs and DIPs, and their downstream signaling cascades in nervous system development. Understanding these mechanisms will also contribute to our understanding of neurological diseases marked by alternations in connectivity such as autism spectrum disorder.

    Neuromuscular system: The larval neuromuscular circuit is highly stereotyped with single cell resolution due to the limited number of motor neurons (35) and muscle targets (30) in each hemisegment. Motor neurons in the ventral nerve cord must send their axons into the periphery and innervate their appropriate muscle target(s) in a highly stereotypic pattern. This system provides an ideal platform in which to tease apart the molecular determinants that contribute to this hard-wired specificity. We recently found that a Dpr-DIP pair controls the targeting of a specific motor neuron to its corresponding muscle. This unique phenotype will serve as a model to delve deeper into the molecules and mechanisms that function in Dpr-DIP regulated wiring using a combination of forward and reverse genetics, biochemistry, electrophysiology, behavioral assays, and cell culture studies.

    Ventral nerve cord: Upstream of muscle innervation, motor neurons receive input from interneurons in the ventral nerve cord (VNC; analogous to the vertebrate spinal cord). These interneurons integrate information from the central brain as well as sensory input in order to produce an appropriate motor response. Here we ask: does interneuron-motor neuron connectivity use similar mechanisms to those used in the neuromuscular system? Unlike the NMJ, these neuronal processes are not sparse enough to allow for single-cell resolution. However, we will utilize genetic tools that allow for single cell resolution of dendritic arbors and axon terminals when combined with confocal microscopy. Simultaneous optogenetic manipulation and calcium imagining, in addition to electrophysiology, will allow us to monitor perturbations in circuit function.

    Visual system: The fly visual circuit is composed of the retina, lamina, medulla, lobula, and lobula plate. Photoreceptors in the retina receive light stimuli and relay signals to downstream neurons which integrate that information to elicit an appropriate behavioral response. The laminar organization of synaptic connections, complete EM reconstruction of the fly brain, and a myriad of genetic tools provide an excellent system to interrogate the mechanisms underlying neural wiring. Dprs and DIPs are expressed in subsets of neurons in the visual circuit and synaptic partners express corresponding Dpr-DIP interacting pairs. Utilizing genetic and functional tools, we are investigating if Dpr-DIP combinations provide a cell-surface signature to specify synaptic partner matching.

    Collapse Biography 
    Collapse education and training
    University of California, Los Angeles, Los AngelesBS06/2001Cybernetics
    Yale School of Medicine, New Haven, CTPhD12/2009Pharmacology
    Collapse awards and honors
    2005 - 2008Ford Foundation Predoctoral Fellowship, Yale
    1998 - 2001NIH/MARC Fellowship, UCLA

    Collapse Research 
    Collapse research activities and funding
    R01NS123439     (CARRILLO, ROBERT ARNULFO)Jun 1, 2021 - May 31, 2026
    IgSF protein interactions drive specificity in circuit wiring and synaptic elaboration
    Role: Principal Investigator

    K01NS102342     (CARRILLO, ROBERT ARNULFO)Jul 1, 2017 - May 31, 2020
    Interactions Between IgSF Proteins in Neural Circuit Formation
    Role: Principal Investigator

    Collapse Bibliographic 
    Collapse selected publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
    Newest   |   Oldest   |   Most Cited   |   Most Discussed   |   Timeline   |   Field Summary   |   Plain Text
    PMC Citations indicate the number of times the publication was cited by articles in PubMed Central, and the Altmetric score represents citations in news articles and social media. (Note that publications are often cited in additional ways that are not shown here.) Fields are based on how the National Library of Medicine (NLM) classifies the publication's journal and might not represent the specific topic of the publication. Translation tags are based on the publication type and the MeSH terms NLM assigns to the publication. Some publications (especially newer ones and publications not in PubMed) might not yet be assigned Field or Translation tags.) Click a Field or Translation tag to filter the publications.
    1. Lobb-Rabe M, Nawrocka WI, Zhang R, Ashley J, Carrillo RA, Özkan E, Lobb-Rabe M, Nawrocka WI, Zhang R, Ashley J, Carrillo RA, Özkan E. Neuronal Wiring Receptors Dprs and DIPs Are GPI Anchored and This Modification Contributes to Their Cell Surface Organization. eNeuro. 2024 Feb; 11(2). PMID: 38233143; PMCID: PMC10863630.
      Citations:    Fields:    Translation:AnimalsCells
    2. Wang Y, Salazar R, Simonetta L, Sorrentino V, Gatton TJ, Wu B, Vecsey CG, Carrillo RA, Wang Y, Salazar R, Simonetta L, Sorrentino V, Gatton TJ, Wu B, Vecsey CG, Carrillo RA. hkb is required for DIP-a expression and target recognition in the Drosophila neuromuscular circuit. bioRxiv. 2023 Oct 17. PMID: 37905128; PMCID: PMC10614772.
    3. Wang Y, Zhang R, Huang S, Valverde PTT, Lobb-Rabe M, Ashley J, Venkatasubramanian L, Carrillo RA. Glial Draper signaling triggers cross-neuron plasticity in bystander neurons after neuronal cell death in Drosophila. Nat Commun. 2023 07 24; 14(1):4452. PMID: 37488133; PMCID: PMC10366216.
      Citations:    Fields:    Translation:AnimalsCells
    4. Wang Y, Zhang R, Huang S, Valverde PT, Lobb-Rabe M, Ashley J, Venkatasubramanian L, Carrillo RA. Glial Draper signaling triggers cross-neuron plasticity in bystander neurons after neuronal cell death. bioRxiv. 2023 Apr 10. PMID: 37090512; PMCID: PMC10120647.
    5. Lobb-Rabe M, DeLong K, Salazar RJ, Zhang R, Wang Y, Carrillo RA. Dpr10 and Nocte are required for Drosophila motor axon pathfinding. Neural Dev. 2022 10 21; 17(1):10. PMID: 36271407; PMCID: PMC9585758.
      Citations: 7     Fields:    Translation:AnimalsCells
    6. Wang Y, Lobb-Rabe M, Ashley J, Chatterjee P, Anand V, Bellen HJ, Kanca O, Carrillo RA. Systematic expression profiling of Dpr and DIP genes reveals cell surface codes in Drosophila larval motor and sensory neurons. Development. 2022 05 15; 149(10). PMID: 35502740; PMCID: PMC9188756.
      Citations: 7     Fields:    Translation:AnimalsCells
    7. Wang Y, Lobb-Rabe M, Ashley J, Anand V, Carrillo RA. Structural and Functional Synaptic Plasticity Induced by Convergent Synapse Loss in the Drosophila Neuromuscular Circuit. J Neurosci. 2021 02 17; 41(7):1401-1417. PMID: 33402422; PMCID: PMC7896011.
      Citations: 11     Fields:    Translation:AnimalsCells
    8. Meng JL, Wang Y, Carrillo RA, Heckscher ES. Temporal transcription factors determine circuit membership by permanently altering motor neuron-to-muscle synaptic partnerships. Elife. 2020 05 11; 9. PMID: 32391795; PMCID: PMC7242025.
      Citations: 8     Fields:    Translation:AnimalsCells
    9. Politano SF, Salemme RR, Ashley J, Bakula TA, Puhalla KA, Quinn JP, Juszczak MJ, Phillip LK, Carrillo RA, Vanderzalm PJ, López-Rivera JA. Tao Negatively Regulates BMP Signaling During Neuromuscular Junction Development in Drosophila. Dev Neurobiol. 2019 04; 79(4):335-349. PMID: 31002474; PMCID: PMC6848449.
      Citations: 4     Fields:    Translation:AnimalsCells
    10. Ashley J, Sorrentino V, Lobb-Rabe M, Nagarkar-Jaiswal S, Tan L, Xu S, Xiao Q, Zinn K, Carrillo RA. Transsynaptic interactions between IgSF proteins DIP-a and Dpr10 are required for motor neuron targeting specificity. Elife. 2019 02 04; 8. PMID: 30714906; PMCID: PMC6391064.
      Citations: 28     Fields:    Translation:AnimalsCells
    11. Cheng S, Ashley J, Kurleto JD, Lobb-Rabe M, Park YJ, Carrillo RA, Özkan E. Molecular basis of synaptic specificity by immunoglobulin superfamily receptors in Drosophila. Elife. 2019 01 28; 8. PMID: 30688651; PMCID: PMC6374074.
      Citations: 20     Fields:    Translation:AnimalsCells
    12. Transsynaptic interactions between IgSF proteins DIP-α and Dpr10 are required for motor neuron targeting specificity in Drosophila. BioRxiv. 2018. View Publication.
    13. Carrillo RA, Menon KP, Nagarkar-Jaiswal S, Lee PT, Jeon M, Birnbaum ME, Bellen HJ, Garcia KC, Zinn K, Özkan E. Control of Synaptic Connectivity by a Network of Drosophila IgSF Cell Surface Proteins. Cell. 2015 Dec 17; 163(7):1770-1782. PMID: 26687361; PMCID: PMC4720259.
      Citations: 79     Fields:    Translation:AnimalsCells
    14. Menon KP, Carrillo RA, Zinn K. The translational regulator Cup controls NMJ presynaptic terminal morphology. Mol Cell Neurosci. 2015 Jul; 67:126-36. PMID: 26102195; PMCID: PMC4540612.
      Citations: 10     Fields:    Translation:AnimalsCells
    15. Carrillo RA, Eastman CL, Weiszmann R, Waghray D, Johnson KG, Zinn K, Celniker SE, Garcia KC, Özkan E. An extracellular interactome of immunoglobulin and LRR proteins reveals receptor-ligand networks. Cell. 2013 Jul 03; 154(1):228-39. PMID: 23827685; PMCID: PMC3756661.
      Citations: 109     Fields:    Translation:AnimalsCells
    16. Carrillo RA, Menon K, Zinn K. Is instability good for the brain? Neuron. 2013 Feb 20; 77(4):599-601. PMID: 23439113.
      Citations: 4     Fields:    Translation:HumansCells
    17. Menon KP, Carrillo RA, Zinn K. Development and plasticity of the Drosophila larval neuromuscular junction. Wiley Interdiscip Rev Dev Biol. 2013 Sep-Oct; 2(5):647-70. PMID: 24014452; PMCID: PMC3767937.
      Citations: 127     Fields:    Translation:AnimalsCells
    18. Carrillo RA, Olsen DP, Yoon KS, Keshishian H. Presynaptic activity and CaMKII modulate retrograde semaphorin signaling and synaptic refinement. Neuron. 2010 Oct 06; 68(1):32-44. PMID: 20920789; PMCID: PMC2950831.
      Citations: 38     Fields:    Translation:AnimalsCells
    19. Mosca TJ, Carrillo RA, White BH, Keshishian H. Dissection of synaptic excitability phenotypes by using a dominant-negative Shaker K+ channel subunit. Proc Natl Acad Sci U S A. 2005 Mar 01; 102(9):3477-82. PMID: 15728380; PMCID: PMC552910.
      Citations: 42     Fields:    Translation:AnimalsCells
    20. Carrillo R, Thiemann OH, Alfonzo JD, Simpson L. Uridine insertion/deletion RNA editing in Leishmania tarentolae mitochondria shows cell cycle dependence. Mol Biochem Parasitol. 2001 Mar; 113(1):175-81. PMID: 11254966.
      Citations: 2     Fields:    Translation:AnimalsCells
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