The interaction between cannabis use and a CB1-related polygenic co-expression index modulates dorsolateral prefrontal activity during working memory processing.
CNR1
Cannabis
Co-expression network
DLPFC
Working memory
Journal
Brain imaging and behavior
ISSN: 1931-7565
Titre abrégé: Brain Imaging Behav
Pays: United States
ID NLM: 101300405
Informations de publication
Date de publication:
Feb 2021
Feb 2021
Historique:
pubmed:
4
3
2020
medline:
28
4
2021
entrez:
4
3
2020
Statut:
ppublish
Résumé
Convergent findings indicate that cannabis use and variation in the cannabinoid CB1 receptor coding gene (CNR1) modulate prefrontal function during working memory (WM). Other results also suggest that cannabis modifies the physiological relationship between genetically induced expression of CNR1 and prefrontal WM processing. However, it is possible that cannabis exerts its modifying effect on prefrontal physiology by interacting with complex molecular ensembles co-regulated with CB1. Since co-regulated genes are likely co-expressed, we investigated how genetically predicted co-expression of a molecular network including CNR1 interacts with cannabis use in modulating WM processing in humans. Using post-mortem human prefrontal data, we first computed a polygenic score (CNR1-PCI), combining the effects of single nucleotide polymorphisms (SNPs) on co-expression of a cohesive gene set including CNR1, and positively correlated with such co-expression. Then, in an in vivo study, we computed CNR1-PCI in 88 cannabis users and 147 non-users and investigated its interaction with cannabis use on brain activity during WM. Results revealed an interaction between cannabis use and CNR1-PCI in the dorsolateral prefrontal cortex (DLPFC), with a positive relationship between CNR1-PCI and DLPFC activity in cannabis users and a negative relationship in non-users. Furthermore, DLPFC activity in cannabis users was positively correlated with the frequency of cannabis use. Taken together, our results suggest that co-expression of a CNR1-related network predicts WM-related prefrontal activation as a function of cannabis use. Furthermore, they offer novel insights into the biological mechanisms associated with the use of cannabis.
Identifiants
pubmed: 32124274
doi: 10.1007/s11682-020-00256-z
pii: 10.1007/s11682-020-00256-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
288-299Subventions
Organisme : Fondazione CON IL SUD
ID : 2011-PDR-06
Organisme : National Alliance for Research on Schizophrenia and Depression
ID : 28935
Organisme : Ricerca Finalizzata
ID : PE-2011-02347951
Références
Ashburner, J., & Friston, K. J. (1999). Nonlinear spatial normalization using basis functions. Human brain Mapping, 7(4), 254–266.
pubmed: 10408769
pmcid: 6873340
Barkus, E. J., Stirling, J., Hopkins, R. S., & Lewis, S. (2006). Cannabis-induced psychosis-like experiences are associated with high schizotypy. Psychopathology, 39(4), 175–178.
pubmed: 16636640
Batalla, A., Bhattacharyya, S., Yücel, M., Fusar-Poli, P., Crippa, J. A., et al. (2013). Structural and functional imaging studies in chronic Cannabis users: A systematic review of adolescent and adult findings. PLoS One, 8(2), e55821.
pubmed: 23390554
pmcid: 3563634
Berghuis, P., Rajnicek, A. M., Morozov, Y. M., Ross, R. A., Mulder, J., Urbán, G. M., Monory, K., Marsicano, G., Matteoli, M., Canty, A., Irving, A. J., Katona, I., Yanagawa, Y., Rakic, P., Lutz, B., Mackie, K., & Harkany, T. (2007). Hardwiring the brain: Endocannabinoids shape neuronal connectivity. Science., 316(5828), 1212–1216.
pubmed: 17525344
Bertolino A., Blasi G. (2009) The genetics of schizophrenia. Neuroscience 164 (1):288-299
Blasi, G., De Virgilio, C., Papazacharias, A., Taurisano, P., Gelao, B., Fazio, L., Ursini, G., Sinibaldi, L., Andriola, I., Masellis, R., Romano, R., Rampino, A., Di Giorgio, A., Lo Bianco, L., Caforio, G., Piva, F., Popolizio, T., Bellantuono, C., Todarello, O., Kleinman, J. E., Gadaleta, G., Weinberger, D. R., & Bertolino, A. (2013). Converging evidence for the association of functional genetic variation in the serotonin receptor 2a gene with prefrontal function and olanzapine treatment. JAMA Psychiatry., 70(9), 921–930.
pubmed: 23842608
Bossong, M. G., Jager, G., van Hell, H. H., Zuurman, L., Jansma, J. M., Mehta, M. A., van Gerven, J. M., Kahn, R. S., & Ramsey, N. F. (2012). Effects of Delta9-tetrahydrocannabinol administration on human encoding and recall memory function: A pharmacological FMRI study. Journal of Cognitive Neuroscience, 24, 588–599.
pubmed: 22066583
Callicott, J. H., Bertolino, A., Mattay, V. S., Langheim, F. J., Duyn, J., Coppola, R., Goldberg, T. E., & Weinberger, D. R. (2000). Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cerebral Cortex., 10(11), 1078–1092.
pubmed: 11053229
Callicott, J. H., Egan, M. F., Mattay, V. S., Bertolino, A., Bone, A. D., Verchinksi, B., & Weinberger, D. R. (2003). Abnormal fMRI response of the dorsolateral prefrontal cortex in cognitively intact siblings of patients with schizophrenia. American Journal of Psychiatry, 160(4), 709–719.
Caspi, A., Moffitt, T. E., Cannon, M., McClay, J., Murray, R., Harrington, H., Taylor, A., Arseneault, L., Williams, B., Braithwaite, A., Poulton, R., & Craig, I. W. (2005). Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: Longitudinal evidence of a gene X environment interaction. Biological Psychiatry, 57(10), 1117–1127.
pubmed: 15866551
Colantuoni, C., Lipska, B. K., Ye, T., Hyde, T. M., Tao, R., Leek, J. T., Colantuoni, E. A., Elkahloun, A. G., Herman, M. M., Weinberger, D. R., & Kleinman, J. E. (2011). Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature, 478(7370), 519–523.
pubmed: 22031444
pmcid: 3510670
Colizzi, M., Fazio, L., Ferranti, L., Porcelli, A., Masellis, R., Marvulli, D., Bonvino, A., Ursini, G., Blasi, G., & Bertolino, A. (2015). Functional genetic variation of the cannabinoid receptor 1 and cannabis use interact on prefrontal connectivity and related working memory behavior. Neuropsychopharmacology, 40(3), 640–649.
pubmed: 25139064
Crane, N. A., Schuster, R. M., Fusar-Poli, P., & Gonzalez, R. (2013). Effects of cannabis on neurocognitive functioning: Recent advances, neurodevelopmental influences, and sex differences. Neuropsychology Review, 23(2), 117–137.
pubmed: 23129391
Di Forti, M., Morgan, C., Dazzan, P., Pariante, C., Mondelli, V., Marques, T. R., Handley, R., Luzi, S., Russo, M., Paparelli, A., Butt, A., Stilo, S. A., Wiffen, B., Powell, J., & Murray, R. M. (2009). High-potency cannabis and the risk of psychosis. British Journal of Psychiatry, 195(6), 488–491.
Eisen, M. B., Spellman, P. T., Brown, P. O., & Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Science of the USA, 95(25), 14863–14868.
Fazio, L., Pergola, G., Papalino, M., Di Carlo, P., Monda, A., Gelao, B., Amoroso, N., Tangaro, S., Rampino, A., Popolizio, T., Bertolino, A., & Blasi, G. (2018). Transcriptomic context of DRD1 is associated with prefrontal activity and behavior during working memory. Proceedings of the National Academy of Sciences of the United States of America, 115(21), 5582–5587.
pubmed: 29735686
pmcid: 6003490
First, M. B., Gibbon, M., Spitzer, R. L., & Williams, J. B. W. (1996). Guide for the structured clinical interview for DSM-IV Axis I disorders-research version. New York: Biometrics Research.
Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., & Turner, R. (1996). Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine, 35(3), 346–355.
pubmed: 8699946
Fromer, M., Roussos, P., Sieberts, S. K., Johnson, J. S., Kavanagh, D. H., Perumal, T. M., Ruderfer, D. M., Oh, E. C., Topol, A., Shah, H. R., Klei, L. L., Kramer, R., Pinto, D., Gümüş, Z. H., Cicek, A. E., Dang, K. K., Browne, A., Lu, C., Xie, L., Readhead, B., Stahl, E. A., Xiao, J., Parvizi, M., Hamamsy, T., Fullard, J. F., Wang, Y. C., Mahajan, M. C., Derry, J. M., Dudley, J. T., Hemby, S. E., Logsdon, B. A., Talbot, K., Raj, T., Bennett, D. A., De Jager, P. L., Zhu, J., Zhang, B., Sullivan, P. F., Chess, A., Purcell, S. M., Shinobu, L. A., Mangravite, L. M., Toyoshiba, H., Gur, R. E., Hahn, C. G., Lewis, D. A., Haroutunian, V., Peters, M. A., Lipska, B. K., Buxbaum, J. D., Schadt, E. E., Hirai, K., Roeder, K., Brennand, K. J., Katsanis, N., Domenici, E., Devlin, B., & Sklar, P. (2016). Gene expression elucidates functional impact of polygenic risk for schizophrenia. Nature Neuroscience, 19(11), 1442–1453.
pubmed: 27668389
pmcid: 5083142
Fukuda, T., Nagashima, S., Abe, T., Kiyonari, H., Inatome, R., & Yanagi, S. (2016). Rescue of CAMDI deletion-induced delayed radial migration and psychiatric behaviors by HDAC6 inhibitor. EMBO reports, 17(12), 1785–1798.
pubmed: 27737934
pmcid: 5283595
Gaiteri, C., Ding, Y., French, B., Tseng, G. C., & Sibille, E. (2014). Beyond modules and hubs: The potential of gene coexpression networks for investigating molecular mechanisms of complex brain disorders. Genes Brain and Behavior, 13(1), 13–24.
Ganzer, F., Br Ning, S., Kraft, S., Sack, P.-M., & Thomasius, R. (2016). Weighing the evidence: A systematic review on long-term neurocognitive effects of cannabis use in abstinent adolescents and adults. Neuropsychology Review, 26(2), 186–222.
pubmed: 27125202
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., Nugent 3rd, T. F., Herman, D. H., Clasen, L. S., Toga, A. W., Rapoport, J. L., & Thompson, P. M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America, 101(21), 8174–8179.
pubmed: 15148381
pmcid: 419576
Herkenham, M., Lynn, A. B., Johnson, M. R., Melvin, L. S., de Costa, B. R., & Rice, K. C. (1991). Characterization and localization of cannabinoid receptors in rat brain: A quantitative in vitro autoradiographic study. Journal of Neuroscience, 11(2), 563–583.
pubmed: 1992016
Jacobus, J., & Tapert, S. F. (2014). Effects of cannabis on the adolescent brain. Current Pharmaceutical Design, 20(13), 2186–2193.
pubmed: 23829363
pmcid: 3930618
Koleske, A. J. (2013). Molecular mechanisms of dendrite stability. Nature Reviews Neuroscience, 14(8), 536–550.
pubmed: 23839597
pmcid: 3947514
Lancichinetti, A., & Fortunato, S. (2012). Consensus clustering in complex networks. Scientific Reports, 2, 2012.
Lisdahl, K. M., & Price, J. S. (2012). Increased marijuana use and gender predict poorer cognitive functioning in adolescents and emerging adults. Journal of the International Neuropsychological Society, 18(4), 678–688. https://doi.org/10.1017/S1355617712000276 .
doi: 10.1017/S1355617712000276
pubmed: 22613255
pmcid: 3956124
Lisdahl, K. M., Wright, N. E., Kirchner-Medina, C., Maple, K. E., & Shollenbarger, S. (2014). Considering cannabis: The effects of regular cannabis use on neurocognition in adolescents and young adults. Current Addiction Reports, 1(2), 144–156.
pubmed: 25013751
pmcid: 4084860
Lubman, D. I., Cheetham, A., & Yücel, M. (2015). Cannabis and adolescent brain development. Pharmacology & Therapeutics, 148, 1–16.
Monaco, A., Monda, A., Amoroso, N., Bertolino, A., Blasi, G., Di Carlo, P., Papalino, M., Pergola, G., Tangaro, S., & Bellotti, R. (2018). A complex network approach reveals a pivotal substructure of genes linked to schizophrenia. PLoS One, 13(1), e0190110.
pubmed: 29304112
pmcid: 5755767
Meier, M. H., Caspi, A., Ambler, A., Harrington, H., Houts, R., Keefe, R. S., McDonald, K., Ward, A., Poulton, R., & Moffitt, T. E. (2012). Persistent cannabis users show neuropsychological decline from childhood to midlife. Proceedings of the National Academy of Sciences of the United States of America, 109(40), E2657–E2664.
pubmed: 22927402
pmcid: 3479587
Meier, M. H., Caspi, A., Danese, A., Fisher, H. L., Houts, R., Arseneault, L., & Moffitt, T. E. (2018). Associations between adolescent cannabis use and neuropsychological decline: A longitudinal co-twin control study. Addiction, 113(2), 257–265.
pubmed: 28734078
Monda A, Amoroso N, Altomare Basile TM, Bellotti R, Bertolino A, Blasi G, Di Carlo P, Fanizzi A, La Rocca M, Maggipinto T, Monaco A, Papalino M, Pergola G, Tangaro S (2017) Topological complex networks properties for Gene Community detection strategy: DRD2 case study. Emergent Complexity from Nonlinearity, in Physics, Engineering and the Life Sciences. Springer, Cham, pp.199–208.
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113.
pubmed: 5146491
Pergola, G., Di Carlo, P., Andriola, I., Gelao, B., Torretta, S., Attrotto, M. T., Fazio, L., Raio, A., Albergo, D., Masellis, R., Rampino, A., Blasi, G., & Bertolino, A. (2016). Combined effect of genetic variants in the GluN2B coding gene (GRIN2B) on prefrontal function during working memory performance. Psychological Medicine, 46(6), 1135–1150.
pubmed: 26690829
Pergola, G., Di Carlo, P., D'Ambrosio, E., Gelao, B., Fazio, L., Papalino, M., Monda, A., Scozia, G., Pietrangelo, B., Attrotto, M., Apud, J. A., Chen, Q., Mattay, V. S., Rampino, A., Caforio, G., Weinberger, D. R., Blasi, G., & Bertolino, A. (2017). DRD2 co-expression network and a related polygenic index predict imaging, behavioral and clinical phenotypes linked to schizophrenia. Translational Psychiatry, 7(1), e1006.
pubmed: 28094815
pmcid: 5545721
Pertwee, R. G. (2008). The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol, cannabidiol and delta9-tetrahydrocannabivarin. British Journal of Pharmacology, 153(2), 199–215.
pubmed: 17828291
SalthouseTA, A. T. M., & Berish, D. E. (2003). Executive functioning as a potential mediator of age-related cognitive decline in normal adults. Journal of Experimental Psychology: General, 132(4), 566–594.
Schwarz Gideon, E. (1978). Estimating the dimension of a model. Annals of Statistics, 6(2), 461–464.
Snodgrass, J. G., & Corwin, J. (1988). Pragmatics of measuring recognition memory: Applications to dementia and amnesia. Journal of Experimental Psychology: General, 117, 34–50.
Sobell, L. C., Agrawal, S., Annis, H., Ayala-Velazquez, H., Echeverria, L., Leo, G. I., et al. (2001). Cross-cultural evaluation of two drinking assessment instruments: Alcohol timeline followback and inventory of drinking situations. Substance Use & Misuse, 36(3), 313–331.
Sobell, L. C., Agrawal, S., Sobell, M. B., Leo, G. I., Young, L. J., Cunningham, J. A., & Simco, E. R. (2003). Comparison of a quick drinking screen with the timeline followback for individuals with alcohol problems. Journal of Studies on Alcohol, 64(6), 858–861.
pubmed: 14743950
Taurisano, P., Antonucci, L. A., Fazio, L., Rampino, A., Romano, R., Porcelli, A., Masellis, R., Colizzi, M., Quarto, T., Torretta, S., Di Giorgio, A., Pergola, G., Bertolino, A., & Blasi, G. (2016). Prefrontal activity during working memory is modulated by the interaction of variation in CB1 and COX2 coding genes and correlates with frequency of cannabis use. Cortex, 81, 231–238.
pubmed: 27261878
van Os, J., Kenis, G., & Rutten, B. P. (2010). The environment and schizophrenia. Nature., 468(7321), 203–212.
pubmed: 21068828
Wong, D. F., Kuwabara, H., Horti, A. G., Raymont, V., Brasic, J., Guevara, M., Ye, W., Dannals, R. F., Ravert, H. T., Nandi, A., Rahmim, A., Ming, J. E., Grachev, I., Roy, C., & Cascella, N. (2010). Quantification of cerebral cannabinoid receptors subtype 1 (CB1) in healthy subjects and schizophrenia by the novel PET radioligand [11C]OMAR. Neuroimage, 52(4), 1505–1513.
pubmed: 20406692
pmcid: 6580862
Zhang B, Horvath S (2005). A general framework for weighted gene co-expression network analysis. Statistical Applications in General and Molecular Biology 4: Article17.
Zoghbi, H. Y. (2003). Postnatal neurodevelopmental disorders: Meeting at the synapse? Science., 302(5646), 826–830.
pubmed: 14593168