Epigenetic effects of paternal cocaine on reward stimulus behavior and accumbens gene expression in mice

Yaw, Alexandra M.; Prosser, Rebecca; Jones, Piet C.; Garcia, Benjamin J.; Jacobson, Daniel A.; Glass, J David

doi:10.1016/j.bbr.2019.02.043

Title: Epigenetic effects of paternal cocaine on reward stimulus behavior and accumbens gene expression in mice

Journal Article · Mon Jul 01 00:00:00 EDT 2019 · Behavioural Brain Research

DOI:https://doi.org/10.1016/j.bbr.2019.02.043· OSTI ID:1559673

Yaw, Alexandra M. ^[1]; Prosser, Rebecca ^[2]; Jones, Piet C. ^[2];

^[2];

^[2]; Glass, J David ^[1]

Kent State Univ., Kent, OH (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Paternal cocaine use causes phenotypic alterations in offspring behavior and associated neural processing. In rodents, changes in first generation (F1) offspring include drug reward behavior, circadian timing, and anxiety responses. This study, utilizing a murine (C57BL/6J) oral cocaine model, examines the effects of paternal cocaine exposure on fundamental characteristics of offspring reward responses, including: 1) the extent of cocaine-induced effects after different durations of sire drug withdrawal; 2) sex- and drug-dependent differences in F1 reward preference; 3) effects on second generation (F2) cocaine preference; and 4) corresponding changes in reward area (nucleus accumbens) mRNA expression. We demonstrate that paternal cocaine intake over a single ˜40-day spermatogenic cycle significantly decreased cocaine (but not ethanol or sucrose) preference in a sex-specific manner in F1 mice from sires mated 24h after drug withdrawal. However, F1 offspring of sires bred 4 months after withdrawal did not exhibit altered cocaine preference. Altered cocaine preference also was not observed in F2's. RNASeq analyses of F1 accumbens tissue revealed changes in gene expression in male offspring of cocaine-exposed sires, including many genes not previously linked to cocaine addiction. Enrichment analyses highlight genes linked to CNS development, synaptic signaling, extracellular matrix, and immune function. Expression correlation analyses identified a novel target, Fam19a4, that may negatively regulate many genes in the accumbens, including genes already identified in addiction. Collectively, these results reveal that paternal cocaine effects in F1 offspring may involve temporally limited epigenetic germline effects and identify new genetic targets for addiction research.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1559673

Journal Information:: Behavioural Brain Research, Vol. 367, Issue N/A

Publisher:: ELSEVIERCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 9 works

Citation information provided by
Web of Science

References (112)

Paternal preconception ethanol exposure blunts hypothalamic-pituitary-adrenal axis responsivity and stress-induced excessive fluid intake in male mice Rompala, Gregory R.; Finegersh, Andrey; Homanics, Gregg E. Alcohol, Vol. 53 https://doi.org/10.1016/j.alcohol.2016.03.006	journal	June 2016
Paternal preconception alcohol exposure imparts intergenerational alcohol-related behaviors to male offspring on a pure C57BL/6J background Rompala, Gregory R.; Finegersh, Andrey; Slater, Michelle Alcohol, Vol. 60 https://doi.org/10.1016/j.alcohol.2016.11.001	journal	May 2017
Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress Rodgers, Ali B.; Morgan, Christopher P.; Leu, N. Adrian Proceedings of the National Academy of Sciences, Vol. 112, Issue 44 https://doi.org/10.1073/pnas.1508347112	journal	October 2015
CCN proteins as potential actionable targets in scleroderma Henrot, Pauline; Truchetet, Marie‐Elise; Fisher, Gary Experimental Dermatology https://doi.org/10.1111/exd.13806	journal	December 2018
In Utero and Lactation Exposure of Rats to 1R4F Reference Cigarette Mainstream Smoke: Effect on Prenatal and Postnatal Development Gaworski, C. L. Toxicological Sciences, Vol. 79, Issue 1 https://doi.org/10.1093/toxsci/kfh083	journal	January 2004
Paternal and Maternal Alcohol Consumption: Effects on Offspring in Two Strains of Rats Abel, Ernest L. Alcoholism: Clinical and Experimental Research, Vol. 13, Issue 4 https://doi.org/10.1111/j.1530-0277.1989.tb00373.x	journal	August 1989
Effects of paternal alcohol consumption on pregnancy outcome in rats Abel, Ernest L.; Tan, S. E. Neurotoxicology and Teratology, Vol. 10, Issue 3 https://doi.org/10.1016/0892-0362(88)90016-5	journal	May 1988
Regulatory role of CCN3 in melanoma cell interaction with the extracellular matrix Vallacchi, Viviana; Rodolfo, Monica Cell Adhesion & Migration, Vol. 3, Issue 1 https://doi.org/10.4161/cam.3.1.6836	journal	January 2009
Shaping Synapses by the Neural Extracellular Matrix Ferrer-Ferrer, Maura; Dityatev, Alexander Frontiers in Neuroanatomy, Vol. 12 https://doi.org/10.3389/fnana.2018.00040	journal	May 2018
Effect of Alcohol Consumption on CpG Methylation in the Differentially Methylated Regions of H19 and IG-DMR in Male Gametes-Implications for Fetal Alcohol Spectrum Disorders Ouko, Lillian A.; Shantikumar, Katpaham; Knezovich, Jaysen Alcoholism: Clinical and Experimental Research, Vol. 33, Issue 9 https://doi.org/10.1111/j.1530-0277.2009.00993.x	journal	September 2009
Genome-wide Analysis of Chromatin Regulation by Cocaine Reveals a Role for Sirtuins Renthal, William; Kumar, Arvind; Xiao, Guanghua Neuron, Vol. 62, Issue 3 https://doi.org/10.1016/j.neuron.2009.03.026	journal	May 2009
Cocaine-Induced Chromatin Remodeling Increases Brain-Derived Neurotrophic Factor Transcription in the Rat Medial Prefrontal Cortex, Which Alters the Reinforcing Efficacy of Cocaine Sadri-Vakili, G.; Kumaresan, V.; Schmidt, H. D. Journal of Neuroscience, Vol. 30, Issue 35 https://doi.org/10.1523/JNEUROSCI.2328-10.2010	journal	September 2010
Paternal Alcohol Exposure Reduces Alcohol Drinking and Increases Behavioral Sensitivity to Alcohol Selectively in Male Offspring Finegersh, Andrey; Homanics, Gregg E. PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0099078	journal	June 2014
Fold change rank ordering statistics: a new method for detecting differentially expressed genes Dembélé, Doulaye; Kastner, Philippe BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2105-15-14	journal	January 2014
Nogo receptor is involved in the adhesion of dendritic cells to myelin McDonald, Claire L.; Steinbach, Karin; Kern, Florian Journal of Neuroinflammation, Vol. 8, Issue 1 https://doi.org/10.1186/1742-2094-8-113	journal	January 2011
Epigenetic Readers of Lysine Acetylation Regulate Cocaine-Induced Plasticity Sartor, G. C.; Powell, S. K.; Brothers, S. P. Journal of Neuroscience, Vol. 35, Issue 45 https://doi.org/10.1523/JNEUROSCI.0826-15.2015	journal	November 2015
Characterization of immune cell subsets during the active phase of multiple sclerosis reveals disease and c-Jun N-terminal kinase pathway biomarkers Ferrandi, Chiara; Richard, Fabien; Tavano, Patrizia Multiple Sclerosis Journal, Vol. 17, Issue 1 https://doi.org/10.1177/1352458510381258	journal	September 2010
Regulation of glutamate transporter 1 (GLT-1) gene expression by cocaine self-administration and withdrawal Kim, Ronald; Sepulveda-Orengo, Marian T.; Healey, Kati L. Neuropharmacology, Vol. 128 https://doi.org/10.1016/j.neuropharm.2017.09.019	journal	January 2018
Divergent Prelimbic Cortical Pathways Interact with BDNF to Regulate Cocaine-seeking Giannotti, Giuseppe; Barry, Sarah M.; Siemsen, Ben M. The Journal of Neuroscience, Vol. 38, Issue 42 https://doi.org/10.1523/JNEUROSCI.1332-18.2018	journal	September 2018
WikiPathways: Pathway Editing for the People Pico, Alexander R.; Kelder, Thomas; van Iersel, Martijn P. PLoS Biology, Vol. 6, Issue 7 https://doi.org/10.1371/journal.pbio.0060184	journal	July 2008
Cocaine Alters BDNF Expression and Neuronal Migration in the Embryonic Mouse Forebrain McCarthy, D. M.; Zhang, X.; Darnell, S. B. Journal of Neuroscience, Vol. 31, Issue 38 https://doi.org/10.1523/JNEUROSCI.2944-11.2011	journal	September 2011
Bidirectional Synaptic Structural Plasticity after Chronic Cocaine Administration Occurs through Rap1 Small GTPase Signaling Cahill, Michael E.; Bagot, Rosemary C.; Gancarz, Amy M. Neuron, Vol. 89, Issue 3 https://doi.org/10.1016/j.neuron.2016.01.031	journal	February 2016
Effect of Cocaine on Cell Proliferation in the Cerebral Wall of Monkey Fetuses Lidow, M. S. Cerebral Cortex, Vol. 11, Issue 6 https://doi.org/10.1093/cercor/11.6.545	journal	June 2001
Pituitary Adenylate Cyclase-Activating Peptide in the Bed Nucleus of the Stria Terminalis Mediates Stress-Induced Reinstatement of Cocaine Seeking in Rats Miles, Olivia W.; Thrailkill, Eric A.; Linden, Anne K. Neuropsychopharmacology, Vol. 43, Issue 5 https://doi.org/10.1038/npp.2017.135	journal	June 2017
Parental THC Exposure Leads to Compulsive Heroin-Seeking and Altered Striatal Synaptic Plasticity in the Subsequent Generation Szutorisz, Henrietta; DiNieri, Jennifer A.; Sweet, Eric Neuropsychopharmacology, Vol. 39, Issue 6 https://doi.org/10.1038/npp.2013.352	journal	January 2014
Heparan sulfate: Resilience factor and therapeutic target for cocaine abuse Chen, Jihuan; Kawamura, Tomoya; Sethi, Manveen K. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-13960-6	journal	October 2017
S-adenosylmethionine modifies cocaine-induced DNA methylation and increases locomotor sensitization in mice Anier, Kaili; Zharkovsky, Alexander; Kalda, Anti International Journal of Neuropsychopharmacology, Vol. 16, Issue 9 https://doi.org/10.1017/S1461145713000394	journal	October 2013
Cocaine absorption from the nasal mucosa Bromley, L.; Hayward, A. Anaesthesia, Vol. 43, Issue 5 https://doi.org/10.1111/j.1365-2044.1988.tb09011.x	journal	May 1988
Exposure to opiates in male adolescent rats alters pain perception in the male offspring Pachenari, Narges; Azizi, Hossein; Ghasemi, Elmira Behavioural Pharmacology, Vol. 29, Issue 2 and 3 https://doi.org/10.1097/FBP.0000000000000388	journal	January 2018
TAFA4, a Chemokine-like Protein, Modulates Injury-Induced Mechanical and Chemical Pain Hypersensitivity in Mice Delfini, Marie-Claire; Mantilleri, Annabelle; Gaillard, Stéphane Cell Reports, Vol. 5, Issue 2 https://doi.org/10.1016/j.celrep.2013.09.013	journal	October 2013
Enhanced anxiety in the male offspring of sires that self-administered cocaine: Anxiety in cocaine-sired rats White, Samantha L.; Vassoler, Fair M.; Schmidt, Heath D. Addiction Biology, Vol. 21, Issue 4 https://doi.org/10.1111/adb.12258	journal	April 2015
Consequences of paternal cocaine exposure in mice He, Fang; Lidow, Irina A.; Lidow, Michael S. Neurotoxicology and Teratology, Vol. 28, Issue 2 https://doi.org/10.1016/j.ntt.2005.12.003	journal	March 2006
Inhalational model of cocaine exposure in mice: Neuroteratological effects He, Fang; Lidow, Irina A.; Lidow, Michael S. Neurotoxicology and Teratology, Vol. 28, Issue 2 https://doi.org/10.1016/j.ntt.2005.12.001	journal	March 2006
Cocaine-induced neurodevelopmental deficits and underlying mechanisms: Mechanisms of Prenatal Cocaine-Induced Deficits Martin, Melissa M.; Graham, Devon L.; McCarthy, Deirdre M. Birth Defects Research Part C: Embryo Today: Reviews, Vol. 108, Issue 2 https://doi.org/10.1002/bdrc.21132	journal	June 2016
Reducing the stress of drug administration: implications for the 3Rs Stuart, Sarah A.; Robinson, Emma S. J. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep14288	journal	September 2015
Effects of repeated cocaine administration on dopamine D1 receptor modulation of mesocorticolimbic GABA and glutamate transmission Steketee, Jeffery D.; Liu, Kun Brain Research, Vol. 1698 https://doi.org/10.1016/j.brainres.2018.07.029	journal	November 2018
Do Defective Immune System-Mediated Myelination Processes Increase Postpartum Psychosis Risk? Dazzan, Paola; Fusté, Montserrat; Davies, William Trends in Molecular Medicine, Vol. 24, Issue 11 https://doi.org/10.1016/j.molmed.2018.09.002	journal	November 2018
Chronic exposure to ethanol of male mice before mating produces attention deficit hyperactivity disorder-like phenotype along with epigenetic dysregulation of dopamine transporter expression in mouse offspring: ADHD-Like Phenotype Induced by EtOH Exposure to Sire Mice Kim, Pitna; Choi, Chang Soon; Park, Jin Hee Journal of Neuroscience Research, Vol. 92, Issue 5 https://doi.org/10.1002/jnr.23275	journal	February 2014
Oral cocaine: plasma concentrations and central effects Van Dyke, C.; Jatlow, P.; Ungerer, J. Science, Vol. 200, Issue 4338 https://doi.org/10.1126/science.24895	journal	April 1978
Contributions of Matrix Metalloproteinases to Neural Plasticity, Habituation, Associative Learning and Drug Addiction Wright, John W.; Harding, Joseph W. Neural Plasticity, Vol. 2009 https://doi.org/10.1155/2009/579382	journal	January 2009
Epigenetic modulation of brain gene networks for cocaine and alcohol abuse Farris, Sean P.; Harris, Robert A.; Ponomarev, Igor Frontiers in Neuroscience, Vol. 9 https://doi.org/10.3389/fnins.2015.00176	journal	May 2015
Paternal nicotine exposure defines different behavior in subsequent generation via hyper-methylation of mmu-miR-15b Dai, Jingbo; Wang, Zhaoxia; Xu, Wangjie Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07920-3	journal	August 2017
A Review of the Effects of Prenatal Cocaine Exposure Among School-Aged Children Ackerman, J. P.; Riggins, T.; Black, M. M. PEDIATRICS, Vol. 125, Issue 3 https://doi.org/10.1542/peds.2009-0637	journal	February 2010
Chronic cocaine causes long-term alterations in circadian period and photic entrainment in the mouse Stowie, A. C.; Amicarelli, M. J.; Prosser, R. A. Neuroscience, Vol. 284 https://doi.org/10.1016/j.neuroscience.2014.08.057	journal	January 2015
Regulation of nucleus accumbens transcript levels in mice by early-life social stress and cocaine Lo Iacono, Luisa; Valzania, Alessandro; Visco-Comandini, Federica Neuropharmacology, Vol. 103 https://doi.org/10.1016/j.neuropharm.2015.12.011	journal	April 2016
Reproductive risks of cocaine Rizk, B. Human Reproduction Update, Vol. 2, Issue 1 https://doi.org/10.1093/humupd/2.1.43	journal	January 1996
Effects of Cocaine Hydrochloride on Reproductive Function and Sexual Behavior of Male Rats and on the Behavior of Their Offspring Abel, E. L.; Moore, C.; Waselewsky, D. Journal of Andrology, Vol. 10, Issue 1 https://doi.org/10.1002/j.1939-4640.1989.tb00051.x	journal	January 1989
Genetic background and epigenetic modifications in the core of the nucleus accumbens predict addiction-like behavior in a rat model Flagel, Shelly B.; Chaudhury, Sraboni; Waselus, Maria Proceedings of the National Academy of Sciences, Vol. 113, Issue 20 https://doi.org/10.1073/pnas.1520491113	journal	April 2016
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases Caspi, Ron; Altman, Tomer; Billington, Richard Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1103	journal	November 2013
Paternal alcohol exposure: paradoxical effect in mice and rats Abel, E. L.; Bilitzke, P. Psychopharmacology, Vol. 100, Issue 2 https://doi.org/10.1007/BF02244399	journal	February 1990
Paternal alcohol consumption affects grooming response in rat offspring Abel, Ernest L. Alcohol, Vol. 8, Issue 1 https://doi.org/10.1016/0741-8329(91)91168-2	journal	January 1991
Development of Anxiety-Like Behavior via Hippocampal IGF-2 Signaling in the Offspring of Parental Morphine Exposure: Effect of Enriched Environment Li, Chang-Qi; Luo, Yan-Wei; Bi, Fang-Fang Neuropsychopharmacology, Vol. 39, Issue 12 https://doi.org/10.1038/npp.2014.128	journal	June 2014
Paternal cocaine taking elicits epigenetic remodeling and memory deficits in male progeny Wimmer, M. E.; Briand, L. A.; Fant, B. Molecular Psychiatry, Vol. 22, Issue 11 https://doi.org/10.1038/mp.2017.8	journal	February 2017
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Chronic cocaine-regulated epigenomic changes in mouse nucleus accumbens Feng, Jian; Wilkinson, Matthew; Liu, Xiaochuan Genome Biology, Vol. 15, Issue 4 https://doi.org/10.1186/gb-2014-15-4-r65	journal	January 2014
Male Germline Transmits Fetal Alcohol Adverse Effect on Hypothalamic Proopiomelanocortin Gene Across Generations Govorko, Dmitry; Bekdash, Rola A.; Zhang, Changqing Biological Psychiatry, Vol. 72, Issue 5 https://doi.org/10.1016/j.biopsych.2012.04.006	journal	September 2012
Effects of Long-Term Cocaine Exposure on Spermatogenesis and Fertility in Peripubertal Male Rats George, Valal K.; Li, Haikun; Teloken, Claudio Journal of Urology, Vol. 155, Issue 1 https://doi.org/10.1016/S0022-5347(01)66654-0	journal	January 1996
Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons Lidow, Michael S.; Song, Zan-Min The Journal of Comparative Neurology, Vol. 435, Issue 3 https://doi.org/10.1002/cne.1028	journal	January 2001
Prdm12 Is Induced by Retinoic Acid and Exhibits Anti-proliferative Properties through the Cell Cycle Modulation of P19 Embryonic Carcinoma Cells Yang, Chia-Ming; Shinkai, Yoichi Cell Structure and Function, Vol. 38, Issue 2 https://doi.org/10.1247/csf.13010	journal	January 2013
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
Paternal alcohol consumption in the rat impairs spatial learning performance in male offspring Wozniak, D. F.; Cicero, T. J.; Kettinger, L. Psychopharmacology, Vol. 105, Issue 2 https://doi.org/10.1007/BF02244324	journal	October 1991
Altered reward sensitivity in female offspring of cocaine-exposed fathers Fischer, Delaney K.; Rice, Richard C.; Martinez Rivera, Arlene Behavioural Brain Research, Vol. 332 https://doi.org/10.1016/j.bbr.2017.05.054	journal	August 2017
Synaptic plasticity mediating cocaine relapse requires matrix metalloproteinases Smith, Alexander C. W.; Kupchik, Yonatan M.; Scofield, Michael D. Nature Neuroscience, Vol. 17, Issue 12 https://doi.org/10.1038/nn.3846	journal	October 2014
Bhlhb5 and Prdm8 Form a Repressor Complex Involved in Neuronal Circuit Assembly Ross, Sarah E.; McCord, Alejandra E.; Jung, Cynthia Neuron, Vol. 73, Issue 2 https://doi.org/10.1016/j.neuron.2011.09.035	journal	January 2012
Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads Jiang, Hongshan; Lei, Rong; Ding, Shou-Wei BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2105-15-182	journal	June 2014
Paternal alcohol exposure: developmental and behavioral effects on the offspring of rats Ledig, M.; Misslin, R.; Vogel, E. Neuropharmacology, Vol. 37, Issue 1 https://doi.org/10.1016/S0028-3908(97)00185-8	journal	January 1998
Gene Ontology: tool for the unification of biology Ashburner, Michael; Ball, Catherine A.; Blake, Judith A. Nature Genetics, Vol. 25, Issue 1 https://doi.org/10.1038/75556	journal	May 2000
Perceptions of epigenetics Bird, Adrian Nature, Vol. 447, Issue 7143 https://doi.org/10.1038/nature05913	journal	May 2007
Cocaine Administration and Its Withdrawal Enhance the Expression of Genes Encoding Histone-Modifying Enzymes and Histone Acetylation in the Rat Prefrontal Cortex Sadakierska-Chudy, Anna; Frankowska, Małgorzata; Jastrzębska, Joanna Neurotoxicity Research, Vol. 32, Issue 1 https://doi.org/10.1007/s12640-017-9728-7	journal	April 2017
Epigenetic transgenerational inheritance of altered stress responses Crews, D.; Gillette, R.; Scarpino, S. V. Proceedings of the National Academy of Sciences, Vol. 109, Issue 23 https://doi.org/10.1073/pnas.1118514109	journal	May 2012
H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells Karmodiya, Krishanpal; Krebs, Arnaud R.; Oulad-Abdelghani, Mustapha BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-424	journal	January 2012
TAFA4 Reverses Mechanical Allodynia through Activation of GABAergic Transmission and Microglial Process Retraction Kambrun, Charline; Roca-Lapirot, Olivier; Salio, Chiara Cell Reports, Vol. 22, Issue 11 https://doi.org/10.1016/j.celrep.2018.02.068	journal	March 2018
Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals Jaenisch, Rudolf; Bird, Adrian Nature Genetics, Vol. 33, Issue S3 https://doi.org/10.1038/ng1089	journal	March 2003
Effects of age and gender but not prenatal cocaine on random ratio and delayed spatial alternation responding in rats Markowski, Vincent P.; Cox, Christopher; Preston, Raymond Neurotoxicology and Teratology, Vol. 22, Issue 3 https://doi.org/10.1016/S0892-0362(99)00080-X	journal	May 2000
A BDNF infusion into the medial prefrontal cortex suppresses cocaine seeking in rats: Intra-PFC BDNF decreases cocaine-seeking behavior Berglind, William J.; See, Ronald E.; Fuchs, Rita A. European Journal of Neuroscience, Vol. 26, Issue 3 https://doi.org/10.1111/j.1460-9568.2007.05692.x	journal	July 2007
TAFA: a novel secreted family with conserved cysteine residues and restricted expression in the brain Tom Tang, Y.; Emtage, Peter; Funk, Walter D. Genomics, Vol. 83, Issue 4 https://doi.org/10.1016/j.ygeno.2003.10.006	journal	April 2004
Withdrawal from extended-access cocaine self-administration results in dysregulated functional activity and altered locomotor activity in rats Calipari, Erin S.; Beveridge, Thomas J. R.; Jones, Sara R. European Journal of Neuroscience, Vol. 38, Issue 12 https://doi.org/10.1111/ejn.12381	journal	October 2013
Role of Tet1 and 5-hydroxymethylcytosine in cocaine action Feng, Jian; Shao, Ningyi; Szulwach, Keith E. Nature Neuroscience, Vol. 18, Issue 4 https://doi.org/10.1038/nn.3976	journal	March 2015
Epigenetic mechanisms of drug addiction Nestler, Eric J. Neuropharmacology, Vol. 76 https://doi.org/10.1016/j.neuropharm.2013.04.004	journal	January 2014
Cocaine plasma concentration: relation to physiological and subjective effects in humans Javaid, J.; Fischman, M.; Schuster, C. Science, Vol. 202, Issue 4364 https://doi.org/10.1126/science.694530	journal	October 1978
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
Prenatal Cocaine Exposure Produces Gender-Specific Motor Effects in Aged Rats Markowski, Vincent P.; Cox, Christopher; Weiss, Bernard Neurotoxicology and Teratology, Vol. 20, Issue 1 https://doi.org/10.1016/S0892-0362(97)00076-7	journal	January 1998
A focus on CXCR4 in Alzheimer's disease Li, Hongyan; Wang, Rong Brain Circulation, Vol. 3, Issue 4 https://doi.org/10.4103/bc.bc_13_17	journal	January 2017
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
Nicotine exposure of male mice produces behavioral impairment in multiple generations of descendants McCarthy, Deirdre M.; Morgan, Thomas J.; Lowe, Sarah E. PLOS Biology, Vol. 16, Issue 10 https://doi.org/10.1371/journal.pbio.2006497	journal	October 2018
Central amygdala ERK signaling pathway is critical to incubation of cocaine craving Lu, Lin; Hope, Bruce T.; Dempsey, Jack Nature Neuroscience, Vol. 8, Issue 2 https://doi.org/10.1038/nn1383	journal	January 2005
Cocaine seeking over extended withdrawal periods in rats: different time courses of responding induced by cocaine cues versus cocaine priming over the first 6 months Lu, Lin; Grimm, Jeffrey W.; Dempsey, Jack Psychopharmacology, Vol. 176, Issue 1 https://doi.org/10.1007/s00213-004-1860-4	journal	April 2004
Functional Connectivity of Chronic Cocaine Use Reveals Progressive Neuroadaptations in Neocortical, Striatal, and Limbic Networks Orsini, Caitlin A.; Colon-Perez, Luis M.; Heshmati, Sara C. eneuro, Vol. 5, Issue 4 https://doi.org/10.1523/ENEURO.0081-18.2018	journal	July 2018
Regulation of gene expression and cocaine reward by CREB and ΔFosB McClung, Colleen A.; Nestler, Eric J. Nature Neuroscience, Vol. 6, Issue 11 https://doi.org/10.1038/nn1143	journal	October 2003
Drug-seeking motivation level in male rats determines offspring susceptibility or resistance to cocaine-seeking behaviour Le, Qiumin; Yan, Biao; Yu, Xiangchen Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15527	journal	May 2017
ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks Bindea, Gabriela; Mlecnik, Bernhard; Hackl, Hubert Bioinformatics, Vol. 25, Issue 8 https://doi.org/10.1093/bioinformatics/btp101	journal	February 2009
Paternal ethanol exposure and behavioral abnormities in offspring: Associated alterations in imprinted gene methylation Liang, Fei; Diao, Lei; Liu, Jun Neuropharmacology, Vol. 81 https://doi.org/10.1016/j.neuropharm.2014.01.025	journal	June 2014
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Paternal Cocaine Disrupts Offspring Circadian Clock Function in a Sex-Dependent Manner in Mice Yaw, Alexandra M.; Woodruff, Robert W.; Prosser, Rebecca A. Neuroscience, Vol. 379 https://doi.org/10.1016/j.neuroscience.2018.03.012	journal	May 2018
Acute paternal alcohol use affects offspring development and adult behavior Meek, Leslie R.; Myren, Kirsten; Sturm, Juliane Physiology & Behavior, Vol. 91, Issue 1 https://doi.org/10.1016/j.physbeh.2007.02.004	journal	May 2007
Stability of Cocaine in Aqueous Solution Murray, John B.; Al-Shora, Hasan I. Journal of Clinical Pharmacy and Therapeutics, Vol. 3, Issue 1 https://doi.org/10.1111/j.1365-2710.1978.tb00096.x	journal	January 1978
Nonhuman Primate Model of the Effect of Prenatal Cocaine Exposure on Cerebral Cortical Development Lidow, Michael S. Annals of the New York Academy of Sciences, Vol. 846, Issue 1 https://doi.org/10.1111/j.1749-6632.1998.tb09736.x	journal	June 1998
Epigenetic regulation of neural stem cell fate during corticogenesis MuhChyi, Chai; Juliandi, Berry; Matsuda, Taito International Journal of Developmental Neuroscience, Vol. 31, Issue 6 https://doi.org/10.1016/j.ijdevneu.2013.02.006	journal	March 2013
Cocaine Self-administration Alters Transcriptome-wide Responses in the Brain’s Reward Circuitry Walker, Deena M.; Cates, Hannah M.; Loh, Yong-Hwee E. Biological Psychiatry, Vol. 84, Issue 12 https://doi.org/10.1016/j.biopsych.2018.04.009	journal	December 2018
Overexpression of the Histone Dimethyltransferase G9a in Nucleus Accumbens Shell Increases Cocaine Self-Administration, Stress-Induced Reinstatement, and Anxiety Anderson, Ethan M.; Larson, Erin B.; Guzman, Daniel The Journal of Neuroscience, Vol. 38, Issue 4 https://doi.org/10.1523/JNEUROSCI.1657-17.2017	journal	December 2017
Cocaine Paired Environment Increases SATB2 Levels in the Rat Paraventricular Thalamus Salti, Ahmad; Apostolova, Galina; Kummer, Kai K. Frontiers in Behavioral Neuroscience, Vol. 12 https://doi.org/10.3389/fnbeh.2018.00224	journal	October 2018
The Extracellular Matrix Protein Brevican Limits Time-Dependent Enhancement of Cocaine Conditioned Place Preference Lubbers, Bart R.; Matos, Mariana R.; Horn, Annemarie Neuropsychopharmacology, Vol. 41, Issue 7 https://doi.org/10.1038/npp.2015.361	journal	December 2015
Subtle biobehavioral effects produced by paternal cocaine exposure Killinger, Catherine E.; Robinson, Stacey; Stanwood, Gregg D. Synapse, Vol. 66, Issue 10 https://doi.org/10.1002/syn.21582	journal	July 2012
voom: precision weights unlock linear model analysis tools for RNA-seq read counts Law, Charity W.; Chen, Yunshun; Shi, Wei Genome Biology, Vol. 15, Issue 2 https://doi.org/10.1186/gb-2014-15-2-r29	journal	January 2014
Epigenetic inheritance of a cocaine-resistance phenotype Vassoler, Fair M.; White, Samantha L.; Schmidt, Heath D. Nature Neuroscience, Vol. 16, Issue 1 https://doi.org/10.1038/nn.3280	journal	December 2012
Multisystem multitasking by CXCL12 and its receptors CXCR4 and ACKR3 Murphy, Philip M.; Heusinkveld, Lauren Cytokine, Vol. 109 https://doi.org/10.1016/j.cyto.2017.12.022	journal	September 2018
Parallel distributed computing using Python Dalcin, Lisandro D.; Paz, Rodrigo R.; Kler, Pablo A. Advances in Water Resources, Vol. 34, Issue 9 https://doi.org/10.1016/j.advwatres.2011.04.013	journal	September 2011
Intranasal and oral cocaine kinetics Wilkinson, Paul; Van Dyke, Craig; Jatlow, Peter Clinical Pharmacology and Therapeutics, Vol. 27, Issue 3 https://doi.org/10.1038/clpt.1980.52	journal	March 1980
FAM19A4 is a novel cytokine ligand of formyl peptide receptor 1 (FPR1) and is able to promote the migration and phagocytosis of macrophages Wang, Wenyan; Li, Ting; Wang, Xiaolin Cellular & Molecular Immunology, Vol. 12, Issue 5 https://doi.org/10.1038/cmi.2014.61	journal	August 2014
Cocaine Exposure Modulates Perineuronal Nets and Synaptic Excitability of Fast-Spiking Interneurons in the Medial Prefrontal Cortex Slaker, Megan L.; Jorgensen, Emily T.; Hegarty, Deborah M. eneuro, Vol. 5, Issue 5 https://doi.org/10.1523/ENEURO.0221-18.2018	journal	September 2018
The Effect of Preconception Paternal Alcohol Exposure on Epigenetic Remodeling of the H19 and Rasgrf1 Imprinting Control Regions in Mouse Offspring Knezovich, Jaysen Gregory; Ramsay, Michèle Frontiers in Genetics, Vol. 3 https://doi.org/10.3389/fgene.2012.00010	journal	January 2012
Circadian rhythm and sleep-wake systems share the dynamic extracellular synaptic milieu Cooper, Joanna M.; Halter, Kathryn A.; Prosser, Rebecca A. Neurobiology of Sleep and Circadian Rhythms, Vol. 5 https://doi.org/10.1016/j.nbscr.2018.04.001	journal	June 2018

Cited By (2)

The epigenetic legacy of illicit drugs: developmental exposures and late-life phenotypes Wanner, Nicole M.; Colwell, Mathia L.; Faulk, Christopher Environmental Epigenetics, Vol. 5, Issue 4 https://doi.org/10.1093/eep/dvz022	journal	October 2019
Paternal morphine self-administration produces object recognition memory deficits in female, but not male offspring Ellis, Alexandra S.; Toussaint, Andre B.; Knouse, Melissa C. Psychopharmacology, Vol. 237, Issue 4 https://doi.org/10.1007/s00213-019-05450-6	journal	January 2020