Fabio Papes

Title(s)Associate Adjunct Professor, Pediatrics
SchoolVc-health Sciences-schools
ORCID ORCID Icon0000-0001-5034-4088 Additional info
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    University of Campinas, BrazilB.Sc12/1996Biological Sciences
    University of Campinas, BrazilPh.D03/2001Genetics and Molecular Biology
    Harvard University, Boston, MAPost-doc08/2003Molecular Neuroscience
    Scripps Research, La Jolla, CAPost-doc07/2008Molecular Neuroscience

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    The research activities in my laboratory have been centered around the field of molecular neuroscience, with two main interests, namely, the study of the pathophysiology of neuropsychiatric childhood disorders and the molecular neurobiology of the sense of olfaction. Regarding the first topic, my group is interested in studying neurodevelopmental pediatric diseases that have well-known genetic etiologies, which represents a window of opportunity not only to understand the participation of genes involved in developmental processes, but also to discover pathophysiological mechanisms that can lead to the generation of new therapeutic strategies. Two genetic diseases have been mostly studied by our team: Pitt-Hopkins Syndrome, a childhood genetic disease characterized by severe motor and cognitive delay, caused by haploinsufficiency of the TCF4 gene, which encodes a poorly characterized bHLH transcription factor; and the syndrome related to the CNTNAP2 gene, which has altered phenotypes similar to Pitt-Hopkins Syndrome. The mechanisms by which TCF4 haploinsufficiency results in Pitt-Hopkins Syndrome are not fully understood, nor it is known if the molecular mechanisms behind the disorders caused by mutations in TCF4 and CNTNAP2 have an overlap. We seek to unravel the genetic, molecular, and cellular bases of these disorders, using patient-derived and mutant human cell lines and cerebral organoids as model systems in vitro, as exemplified by the publications below. Our long-term goal is to identify altered pathways that can become pharmacological targets, as well as obtain proof-of-concept that gene therapy strategies can be applied to those disorders.
    Another line of investigation in my lab seeks to decipher the function of olfaction in controlling motivated behaviors, such as reproduction, aggression, territoriality, and parental behavior. My team has used the mouse as a model to explore stereotyped behaviors induced by olfactory stimuli and to understand how these cues are detected by the olfactory sensory organs from a molecular and cellular standpoint. We have also studied the role of hormones, particularly oxytocin, in mediating these behavioral changes and how olfactory information is internally represented and processed in the brain. Numerous collaborations have been established by my group throughout the years, the most fruitful of which have been with Profs. Lisa Stowers (Scripps Research), Darren Logan (Welcome Trust Sanger Institute, UK), and Alysson Muotri (UCSD).

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    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Researchers can login to make corrections and additions, or contact us for help. to make corrections and additions.
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    Altmetrics Details 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. SARS-CoV-2 infects human brain organoids causing cell death and loss of synapses that can be rescued by treatment with Sofosbuvir. PLoS Biol. 2022 11; 20(11):e3001845. Mesci P, de Souza JS, Martin-Sancho L, Macia A, Saleh A, Yin X, Snethlage C, Adams JW, Avansini SH, Herai RH, Almenar-Queralt A, Pu Y, Szeto RA, Goldberg G, Bruck PT, Papes F, Chanda SK, Muotri AR. PMID: 36327326; PMCID: PMC9632769.
      View in: PubMed   Mentions: 16     Fields:    Translation:HumansCells
    2. The impact of antidepressants on human neurodevelopment: Brain organoids as experimental tools. Semin Cell Dev Biol. 2023 07 30; 144:67-76. Marinho LSR, Chiarantin GMD, Ikebara JM, Cardoso DS, de Lima-Vasconcellos TH, Higa GSV, Ferraz MSA, De Pasquale R, Takada SH, Papes F, Muotri AR, Kihara AH. PMID: 36115764.
      View in: PubMed   Mentions: 1     Fields:    Translation:HumansAnimals
    3. Transcription Factor 4 loss-of-function is associated with deficits in progenitor proliferation and cortical neuron content. Nat Commun. 2022 05 02; 13(1):2387. Papes F, Camargo AP, de Souza JS, Carvalho VMA, Szeto RA, LaMontagne E, Teixeira JR, Avansini SH, Sánchez-Sánchez SM, Nakahara TS, Santo CN, Wu W, Yao H, Araújo BMP, Velho PENF, Haddad GG, Muotri AR. PMID: 35501322; PMCID: PMC9061776.
      View in: PubMed   Mentions: 15     Fields:    Translation:HumansCells
    4. Disease-associated mutations in topoisomerase IIβ result in defective NK cells. J Allergy Clin Immunol. 2022 06; 149(6):2171-2176.e3. Broderick L, Clay GM, Blum RH, Liu Y, McVicar R, Papes F, Booshehri LM, Cowell IG, Austin CA, Putnam CD, Kaufman DS. PMID: 35063500.
      View in: PubMed   Mentions: 4     Fields:    Translation:HumansAnimalsCells
    5. Investigation of Activated Mouse Olfactory Sensory Neurons via Combined Immunostaining and in situ Hybridization. J Vis Exp. 2021 04 11; (170). de Andrade Carvalho VM, Seike Nakahara T, Papes F. PMID: 33900298.
      View in: PubMed   Mentions:    Fields:    Translation:AnimalsCells
    6. Transcription factor 4 and its association with psychiatric disorders. Transl Psychiatry. 2021 01 05; 11(1):19. Teixeira JR, Szeto RA, Carvalho VMA, Muotri AR, Papes F. PMID: 33414364; PMCID: PMC7791034.
      View in: PubMed   Mentions: 14     Fields:    Translation:Humans
    7. Peripheral oxytocin injection modulates vomeronasal sensory activity and reduces pup-directed aggression in male mice. Sci Rep. 2020 11 17; 10(1):19943. Nakahara TS, Camargo AP, Magalhães PHM, Souza MAA, Ribeiro PG, Martins-Netto PH, Carvalho VMA, José J, Papes F. PMID: 33203885; PMCID: PMC7673031.
      View in: PubMed   Mentions: 5     Fields:    Translation:Animals
    8. Detection of Activated Mouse Neurons with Temporal Resolution via Dual c-Fos Staining. STAR Protoc. 2020 12 18; 1(3):100153. Nakahara TS, Carvalho VMA, Souza MAA, Trintinalia GZ, Papes F. PMID: 33377047; PMCID: PMC7757322.
      View in: PubMed   Mentions: 1     Fields:    Translation:AnimalsCells
    9. Representation of Olfactory Information in Organized Active Neural Ensembles in the Hypothalamus. Cell Rep. 2020 08 25; 32(8):108061. Carvalho VMA, Nakahara TS, Souza MAA, Cardozo LM, Trintinalia GZ, Pissinato LG, Venancio JO, Stowers L, Papes F. PMID: 32846119.
      View in: PubMed   Mentions: 10     Fields:    Translation:HumansAnimals
    10. From Synapse to Supper: A Food Preference Recipe with Olfactory Synaptic Ingredients. Neuron. 2020 07 08; 107(1):8-11. Nakahara TS, Carvalho VMA, Papes F. PMID: 32645309.
      View in: PubMed   Mentions:    Fields:    Translation:AnimalsCells
    11. Uncovering the mouse olfactory long non-coding transcriptome with a novel machine-learning model. DNA Res. 2019 Aug 01; 26(4):365-378. Camargo AP, Nakahara TS, Firmino LER, Netto PHM, do Nascimento JBP, Donnard ER, Galante PAF, Carazzolle MF, Malnic B, Papes F. PMID: 31321403; PMCID: PMC6704403.
      View in: PubMed   Mentions: 6     Fields:    Translation:AnimalsCells
    12. Behavioral Assays in the Study of Olfaction: A Practical Guide. Methods Mol Biol. 2018; 1820:289-388. Papes F, Nakahara TS, Camargo AP. PMID: 29884953.
      View in: PubMed   Mentions: 4     Fields:    Translation:Animals
    13. The Strange Case of Aggression and the Brain. Neuron. 2017 Aug 16; 95(4):734-737. Carvalho VMA, Nakahara TS, Papes F. PMID: 28817796.
      View in: PubMed   Mentions: 2     Fields:    Translation:HumansAnimals
    14. Variation in olfactory neuron repertoires is genetically controlled and environmentally modulated. Elife. 2017 04 25; 6. Ibarra-Soria X, Nakahara TS, Lilue J, Jiang Y, Trimmer C, Souza MA, Netto PH, Ikegami K, Murphy NR, Kusma M, Kirton A, Saraiva LR, Keane TM, Matsunami H, Mainland J, Papes F, Logan DW. PMID: 28438259; PMCID: PMC5404925.
      View in: PubMed   Mentions: 42     Fields:    Translation:AnimalsCells
    15. CD36 is expressed in a defined subpopulation of neurons in the olfactory epithelium. Sci Rep. 2016 05 05; 6:25507. Xavier AM, Ludwig RG, Nagai MH, de Almeida TJ, Watanabe HM, Hirata MY, Rosenstock TR, Papes F, Malnic B, Glezer I. PMID: 27145700; PMCID: PMC4857125.
      View in: PubMed   Mentions: 11     Fields:    Translation:AnimalsCells
    16. Detection of pup odors by non-canonical adult vomeronasal neurons expressing an odorant receptor gene is influenced by sex and parenting status. BMC Biol. 2016 Feb 15; 14:12. Nakahara TS, Cardozo LM, Ibarra-Soria X, Bard AD, Carvalho VM, Trintinalia GZ, Logan DW, Papes F. PMID: 26878847; PMCID: PMC4753656.
      View in: PubMed   Mentions: 8     Fields:    Translation:AnimalsCells
    17. Lack of spatial segregation in the representation of pheromones and kairomones in the mouse medial amygdala. Front Neurosci. 2015; 9:283. Carvalho VM, Nakahara TS, Cardozo LM, Souza MA, Camargo AP, Trintinalia GZ, Ferraz E, Papes F. PMID: 26321906; PMCID: PMC4531233.
      View in: PubMed   Mentions: 10  
    18. The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell. 2010 May 14; 141(4):692-703. Papes F, Logan DW, Stowers L. PMID: 20478258; PMCID: PMC2873972.
      View in: PubMed   Mentions: 152     Fields:    Translation:Animals
    19. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell. 2003 Mar 07; 112(5):607-18. Loconto J, Papes F, Chang E, Stowers L, Jones EP, Takada T, Kumánovics A, Fischer Lindahl K, Dulac C. PMID: 12628182.
      View in: PubMed   Mentions: 102     Fields:    Translation:AnimalsCells
    20. The essential amino acid lysine acts as precursor of glutamate in the mammalian central nervous system. FEBS Lett. 2001 Jan 12; 488(1-2):34-8. Papes F, Surpili MJ, Langone F, Trigo JR, Arruda P. PMID: 11163791.
      View in: PubMed   Mentions: 33     Fields:    Translation:AnimalsCells
    21. Regulation of lysine catabolism in higher plants. Trends Plant Sci. 2000 Aug; 5(8):324-30. Arruda P, Kemper EL, Papes F, Leite A. PMID: 10908876.
      View in: PubMed   Mentions: 46     Fields:    Translation:Animals
    22. The role of opaque2 in the control of lysine-degrading activities in developing maize endosperm. Plant Cell. 1999 Oct; 11(10):1981-94. Kemper EL, Neto GC, Papes F, Moraes KC, Leite A, Arruda P. PMID: 10521527; PMCID: PMC144114.
      View in: PubMed   Mentions: 49     Fields:    Translation:AnimalsCells
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