A Genome-wide Screen Identifies PAPP-AA-Mediated IGFR Signaling as a Novel Regulator of Habituation Learning
Habituation represents a fundamental form of learning, yet the underlying molecular genetic mechanisms are not well defined. Here we report on a genome-wide genetic screen, coupled with whole-genome sequencing, that identified 14 zebrafish startle habituation mutants including mutants of the vertebr...
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| Published in | Neuron (Cambridge, Mass.) Vol. 85; no. 6; pp. 1200 - 1211 |
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| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
18.03.2015
Elsevier Limited |
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| Online Access | Get full text |
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| Abstract | Habituation represents a fundamental form of learning, yet the underlying molecular genetic mechanisms are not well defined. Here we report on a genome-wide genetic screen, coupled with whole-genome sequencing, that identified 14 zebrafish startle habituation mutants including mutants of the vertebrate-specific gene pregnancy-associated plasma protein-aa (pappaa). PAPP-AA encodes an extracellular metalloprotease known to increase IGF bioavailability, thereby enhancing IGF receptor signaling. We find that pappaa is expressed by startle circuit neurons, and expression of wild-type but not a metalloprotease-inactive version of pappaa restores habituation in pappaa mutants. Furthermore, acutely inhibiting IGF1R function in wild-type reduces habituation, while activation of IGF1R downstream effectors in pappaa mutants restores habituation, demonstrating that pappaa promotes learning by acutely and locally increasing IGF bioavailability. In sum, our results define the first functional gene set for habituation learning in a vertebrate and identify PAPPAA-regulated IGF signaling as a novel mechanism regulating habituation learning.
•Genome-wide genetic screen identifies first set of vertebrate learning mutants•pregnancy-associated plasma protein-aa is a novel regulator of habituation learning•PAPP-AA functions as a metalloprotease to promote habituation•PAPP-AA/IGF1R/PI3K/Akt signaling axis as a pharmacological target for learning
Through a forward genetic screen in zebrafish, Wolman et al. isolate the first functional vertebrate gene set for habituation learning and identify pregnancy-associated plasma protein aa (PAPP-AA)-regulated IGF signaling as a novel mechanism underlying habituation learning. |
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| AbstractList | Habituation represents a fundamental form of learning, yet the underlying molecular genetic mechanisms are not well defined. Here we report on a genome-wide genetic screen, coupled with whole-genome sequencing, that identified 14 zebrafish startle habituation mutants including mutants of the vertebrate-specific genepregnancy-associated plasma protein-aa(pappaa). PAPP-AA encodes an extracellular metalloprotease known to increase IGF bioavailability, thereby enhancing IGF receptor signaling. We find thatpappaais expressed by startle circuit neurons, and expression of wild-type but not a metalloprotease-inactive version ofpappaarestores habituation inpappaamutants. Furthermore, acutely inhibiting IGF1R function in wild-type reduces habituation, while activation of IGF1R downstream effectors inpappaamutants restores habituation, demonstrating thatpappaapromotes learning by acutely and locally increasing IGF bioavailability. In sum, our results define the first functional gene set for habituation learning in a vertebrate and identify PAPPAA-regulated IGF signaling as a novel mechanism regulating habituation learning. Habituation represents a fundamental form of learning, yet the underlying molecular genetic mechanisms are not well defined. Here we report on a genome-wide genetic screen, coupled with whole genome sequencing, that identified 14 zebrafish startle habituation mutants including mutants of the vertebrate specific gene pregnancy associated plasma protein-aa (pappaa) . PAPP-AA encodes an extracellular metalloprotease known to increase IGF bioavailability thereby enhancing IGF receptor signaling. We find that pappaa is expressed by startle circuit neurons, and expression of wildtype, but not a metalloprotease-inactive version of pappaa restores habituation in pappaa mutants. Furthermore, acutely inhibiting IGF1R function in wild-type reduces habituation, while activation of IGF1R downstream effectors in pappaa mutants restores habituation, demonstrating that pappaa promotes learning by acutely and locally increasing IGF bioavailability. In sum, our results define the first functional gene set for habituation learning in a vertebrate, and identify PAPPAA-regulated IGF signaling as a novel mechanism regulating habituation learning. Habituation represents a fundamental form of learning, yet the underlying molecular genetic mechanisms are not well defined. Here we report on a genome-wide genetic screen, coupled with whole-genome sequencing, that identified 14 zebrafish startle habituation mutants including mutants of the vertebrate-specific gene pregnancy-associated plasma protein-aa (pappaa). PAPP-AA encodes an extracellular metalloprotease known to increase IGF bioavailability, thereby enhancing IGF receptor signaling. We find that pappaa is expressed by startle circuit neurons, and expression of wild-type but not a metalloprotease-inactive version of pappaa restores habituation in pappaa mutants. Furthermore, acutely inhibiting IGF1R function in wild-type reduces habituation, while activation of IGF1R downstream effectors in pappaa mutants restores habituation, demonstrating that pappaa promotes learning by acutely and locally increasing IGF bioavailability. In sum, our results define the first functional gene set for habituation learning in a vertebrate and identify PAPPAA-regulated IGF signaling as a novel mechanism regulating habituation learning. Habituation represents a fundamental form of learning, yet the underlying molecular genetic mechanisms are not well defined. Here we report on a genome-wide genetic screen, coupled with whole-genome sequencing, that identified 14 zebrafish startle habituation mutants including mutants of the vertebrate-specific gene pregnancy-associated plasma protein-aa (pappaa). PAPP-AA encodes an extracellular metalloprotease known to increase IGF bioavailability, thereby enhancing IGF receptor signaling. We find that pappaa is expressed by startle circuit neurons, and expression of wild-type but not a metalloprotease-inactive version of pappaa restores habituation in pappaa mutants. Furthermore, acutely inhibiting IGF1R function in wild-type reduces habituation, while activation of IGF1R downstream effectors in pappaa mutants restores habituation, demonstrating that pappaa promotes learning by acutely and locally increasing IGF bioavailability. In sum, our results define the first functional gene set for habituation learning in a vertebrate and identify PAPPAA-regulated IGF signaling as a novel mechanism regulating habituation learning. •Genome-wide genetic screen identifies first set of vertebrate learning mutants•pregnancy-associated plasma protein-aa is a novel regulator of habituation learning•PAPP-AA functions as a metalloprotease to promote habituation•PAPP-AA/IGF1R/PI3K/Akt signaling axis as a pharmacological target for learning Through a forward genetic screen in zebrafish, Wolman et al. isolate the first functional vertebrate gene set for habituation learning and identify pregnancy-associated plasma protein aa (PAPP-AA)-regulated IGF signaling as a novel mechanism underlying habituation learning. |
| Author | Skinner, Julianne Hogenesch, John B. Marsden, Kurt C. Bell, Hannah Jain, Roshan A. Wolman, Marc A. Granato, Michael Hayer, Katharina E. |
| AuthorAffiliation | 3 Department of Zoology, University of Wisconsin; 213 Zoology Research Building, 1117 West Johnson Street, Madison, WI, 53706, USA 1 Department of Cell and Developmental Biology; University of Pennsylvania Perelman School of Medicine; 1157 BRB II/III, 421 Curie Boulevard, Philadelphia, PA, 19104, USA 2 Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine; 829 BRB II/III, 421 Curie Boulevard, Philadelphia, PA, 19104, USA |
| AuthorAffiliation_xml | – name: 3 Department of Zoology, University of Wisconsin; 213 Zoology Research Building, 1117 West Johnson Street, Madison, WI, 53706, USA – name: 1 Department of Cell and Developmental Biology; University of Pennsylvania Perelman School of Medicine; 1157 BRB II/III, 421 Curie Boulevard, Philadelphia, PA, 19104, USA – name: 2 Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine; 829 BRB II/III, 421 Curie Boulevard, Philadelphia, PA, 19104, USA |
| Author_xml | – sequence: 1 givenname: Marc A. surname: Wolman fullname: Wolman, Marc A. organization: Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, 1157 BRB II/III, 421 Curie Boulevard, Philadelphia, PA 19104, USA – sequence: 2 givenname: Roshan A. surname: Jain fullname: Jain, Roshan A. organization: Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, 1157 BRB II/III, 421 Curie Boulevard, Philadelphia, PA 19104, USA – sequence: 3 givenname: Kurt C. surname: Marsden fullname: Marsden, Kurt C. organization: Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, 1157 BRB II/III, 421 Curie Boulevard, Philadelphia, PA 19104, USA – sequence: 4 givenname: Hannah surname: Bell fullname: Bell, Hannah organization: Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, 1157 BRB II/III, 421 Curie Boulevard, Philadelphia, PA 19104, USA – sequence: 5 givenname: Julianne surname: Skinner fullname: Skinner, Julianne organization: Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, 1157 BRB II/III, 421 Curie Boulevard, Philadelphia, PA 19104, USA – sequence: 6 givenname: Katharina E. surname: Hayer fullname: Hayer, Katharina E. organization: Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine, 829 BRB II/III, 421 Curie Boulevard, Philadelphia, PA 19104, USA – sequence: 7 givenname: John B. surname: Hogenesch fullname: Hogenesch, John B. organization: Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine, 829 BRB II/III, 421 Curie Boulevard, Philadelphia, PA 19104, USA – sequence: 8 givenname: Michael surname: Granato fullname: Granato, Michael email: granatom@mail.med.upenn.edu organization: Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, 1157 BRB II/III, 421 Curie Boulevard, Philadelphia, PA 19104, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25754827$$D View this record in MEDLINE/PubMed |
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| Snippet | Habituation represents a fundamental form of learning, yet the underlying molecular genetic mechanisms are not well defined. Here we report on a genome-wide... |
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| SubjectTerms | Animal behavior Animals Behavior, Animal Danio rerio Female Genetic Testing - methods Genome, Archaeal Learning - physiology Mutation Mutation - genetics Neurons - metabolism Pregnancy Pregnancy-Associated Plasma Protein-A - genetics Pregnancy-Associated Plasma Protein-A - metabolism Receptor, IGF Type 1 - genetics Receptor, IGF Type 1 - metabolism Reflexes Rodents Signal Transduction - genetics Zebrafish Zebrafish - metabolism |
| Title | A Genome-wide Screen Identifies PAPP-AA-Mediated IGFR Signaling as a Novel Regulator of Habituation Learning |
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