Escalated (Dependent) Oxycodone Self-Administration Is Associated with Cognitive Impairment and Transcriptional Evidence of Neurodegeneration in Human Immunodeficiency Virus (HIV) Transgenic Rats

Substance use disorder is associated with accelerated disease progression in people with human immunodeficiency virus (HIV; PWH). Problem opioid use, including high-dose opioid therapy, prescription drug misuse, and opioid abuse, is high and increasing in the PWH population. Oxycodone is a broadly p...

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Published in	Viruses Vol. 14; no. 4; p. 669
Main Authors	Fu, Yu, Lorrai, Irene, Zorman, Barry, Mercatelli, Daniele, Shankula, Chase, Marquez Gaytan, Jorge, Lefebvre, Celine, de Guglielmo, Giordano, Kim, Hyunjae Ryan, Sumazin, Pavel, Giorgi, Federico M., Repunte-Canonigo, Vez, Sanna, Pietro Paolo
Format	Journal Article
Language	English
Published	Switzerland MDPI AG 24.03.2022 MDPI
Subjects	Adaptation AIDS Analgesics, Opioid - adverse effects Animals Catheters Cognitive ability Cognitive Dysfunction - chemically induced Cognitive Dysfunction - complications cognitive impairment Drug abuse Drug dosages Drug use Gene expression Glucocorticoids HIV HIV Infections - complications Human immunodeficiency virus Humans Immune system Inflammation Intubation Kinases Laboratory animals Narcotics Neurodegeneration neuroHIV neuroinflammation Neurotoxicity Opioids Oxycodone Oxycodone - adverse effects Pattern recognition Prefrontal cortex Prescription drugs Rats Rats, Transgenic Self-administration Transcription United States > US AIDS cognitive impairment neuroinflammation neuroHIV
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Abstract	Substance use disorder is associated with accelerated disease progression in people with human immunodeficiency virus (HIV; PWH). Problem opioid use, including high-dose opioid therapy, prescription drug misuse, and opioid abuse, is high and increasing in the PWH population. Oxycodone is a broadly prescribed opioid in both the general population and PWH. Here, we allowed HIV transgenic (Tg) rats and wildtype (WT) littermates to intravenously self-administer oxycodone under short-access (ShA) conditions, which led to moderate, stable, “recreational”-like levels of drug intake, or under long-access (LgA) conditions, which led to escalated (dependent) drug intake. HIV Tg rats with histories of oxycodone self-administration under LgA conditions exhibited significant impairment in memory performance in the novel object recognition (NOR) paradigm. RNA-sequencing expression profiling of the medial prefrontal cortex (mPFC) in HIV Tg rats that self-administered oxycodone under ShA conditions exhibited greater transcriptional evidence of inflammation than WT rats that self-administered oxycodone under the same conditions. HIV Tg rats that self-administered oxycodone under LgA conditions exhibited transcriptional evidence of an increase in neuronal injury and neurodegeneration compared with WT rats under the same conditions. Gene expression analysis indicated that glucocorticoid-dependent adaptations contributed to the gene expression effects of oxycodone self-administration. Overall, the present results indicate that a history of opioid intake promotes neuroinflammation and glucocorticoid dysregulation, and excessive opioid intake is associated with neurotoxicity and cognitive impairment in HIV Tg rats.
AbstractList	Substance use disorder is associated with accelerated disease progression in people with human immunodeficiency virus (HIV; PWH). Problem opioid use, including high-dose opioid therapy, prescription drug misuse, and opioid abuse, is high and increasing in the PWH population. Oxycodone is a broadly prescribed opioid in both the general population and PWH. Here, we allowed HIV transgenic (Tg) rats and wildtype (WT) littermates to intravenously self-administer oxycodone under short-access (ShA) conditions, which led to moderate, stable, “recreational”-like levels of drug intake, or under long-access (LgA) conditions, which led to escalated (dependent) drug intake. HIV Tg rats with histories of oxycodone self-administration under LgA conditions exhibited significant impairment in memory performance in the novel object recognition (NOR) paradigm. RNA-sequencing expression profiling of the medial prefrontal cortex (mPFC) in HIV Tg rats that self-administered oxycodone under ShA conditions exhibited greater transcriptional evidence of inflammation than WT rats that self-administered oxycodone under the same conditions. HIV Tg rats that self-administered oxycodone under LgA conditions exhibited transcriptional evidence of an increase in neuronal injury and neurodegeneration compared with WT rats under the same conditions. Gene expression analysis indicated that glucocorticoid-dependent adaptations contributed to the gene expression effects of oxycodone self-administration. Overall, the present results indicate that a history of opioid intake promotes neuroinflammation and glucocorticoid dysregulation, and excessive opioid intake is associated with neurotoxicity and cognitive impairment in HIV Tg rats. Substance use disorder is associated with accelerated disease progression in people with human immunodeficiency virus (HIV; PWH). Problem opioid use, including high-dose opioid therapy, prescription drug misuse, and opioid abuse, is high and increasing in the PWH population. Oxycodone is a broadly prescribed opioid in both the general population and PWH. Here, we allowed HIV transgenic (Tg) rats and wildtype (WT) littermates to intravenously self-administer oxycodone under short-access (ShA) conditions, which led to moderate, stable, "recreational"-like levels of drug intake, or under long-access (LgA) conditions, which led to escalated (dependent) drug intake. HIV Tg rats with histories of oxycodone self-administration under LgA conditions exhibited significant impairment in memory performance in the novel object recognition (NOR) paradigm. RNA-sequencing expression profiling of the medial prefrontal cortex (mPFC) in HIV Tg rats that self-administered oxycodone under ShA conditions exhibited greater transcriptional evidence of inflammation than WT rats that self-administered oxycodone under the same conditions. HIV Tg rats that self-administered oxycodone under LgA conditions exhibited transcriptional evidence of an increase in neuronal injury and neurodegeneration compared with WT rats under the same conditions. Gene expression analysis indicated that glucocorticoid-dependent adaptations contributed to the gene expression effects of oxycodone self-administration. Overall, the present results indicate that a history of opioid intake promotes neuroinflammation and glucocorticoid dysregulation, and excessive opioid intake is associated with neurotoxicity and cognitive impairment in HIV Tg rats.Substance use disorder is associated with accelerated disease progression in people with human immunodeficiency virus (HIV; PWH). Problem opioid use, including high-dose opioid therapy, prescription drug misuse, and opioid abuse, is high and increasing in the PWH population. Oxycodone is a broadly prescribed opioid in both the general population and PWH. Here, we allowed HIV transgenic (Tg) rats and wildtype (WT) littermates to intravenously self-administer oxycodone under short-access (ShA) conditions, which led to moderate, stable, "recreational"-like levels of drug intake, or under long-access (LgA) conditions, which led to escalated (dependent) drug intake. HIV Tg rats with histories of oxycodone self-administration under LgA conditions exhibited significant impairment in memory performance in the novel object recognition (NOR) paradigm. RNA-sequencing expression profiling of the medial prefrontal cortex (mPFC) in HIV Tg rats that self-administered oxycodone under ShA conditions exhibited greater transcriptional evidence of inflammation than WT rats that self-administered oxycodone under the same conditions. HIV Tg rats that self-administered oxycodone under LgA conditions exhibited transcriptional evidence of an increase in neuronal injury and neurodegeneration compared with WT rats under the same conditions. Gene expression analysis indicated that glucocorticoid-dependent adaptations contributed to the gene expression effects of oxycodone self-administration. Overall, the present results indicate that a history of opioid intake promotes neuroinflammation and glucocorticoid dysregulation, and excessive opioid intake is associated with neurotoxicity and cognitive impairment in HIV Tg rats.
Author	Mercatelli, Daniele Sumazin, Pavel Sanna, Pietro Paolo Fu, Yu Shankula, Chase Zorman, Barry Lefebvre, Celine Kim, Hyunjae Ryan de Guglielmo, Giordano Marquez Gaytan, Jorge Giorgi, Federico M. Repunte-Canonigo, Vez Lorrai, Irene
AuthorAffiliation	2 European Bioinformatics Institute (EMBL-EBI), Hinxton CB10 1SD, UK 6 Department of Psychiatry, University of California, La Jolla, San Diego, CA 92093, USA; gdeguglielmo@ucsd.edu 4 Department of Pharmacy and Biotechnology, University of Bologna, 40126 Bologna, Italy; danielemercatelli@gmail.com (D.M.); federico.giorgi@unibo.it (F.M.G.) 1 Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, San Diego, CA 92037, USA; fuyu0413@gmail.com (Y.F.); ilorrai@scripps.edu (I.L.); cshankula@scripps.edu (C.S.); jmarquez@scripps.edu (J.M.G.); celinelef@gmail.com (C.L.) 5 92160 Antony, France 3 Department of Pediatrics, Dan L. Duncan Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA; barry.zorman@bcm.edu (B.Z.); ryan.kim2112@gmail.com (H.R.K.); pavel.sumazin@bcm.edu (P.S.)
AuthorAffiliation_xml	– name: 5 92160 Antony, France – name: 4 Department of Pharmacy and Biotechnology, University of Bologna, 40126 Bologna, Italy; danielemercatelli@gmail.com (D.M.); federico.giorgi@unibo.it (F.M.G.) – name: 6 Department of Psychiatry, University of California, La Jolla, San Diego, CA 92093, USA; gdeguglielmo@ucsd.edu – name: 2 European Bioinformatics Institute (EMBL-EBI), Hinxton CB10 1SD, UK – name: 3 Department of Pediatrics, Dan L. Duncan Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA; barry.zorman@bcm.edu (B.Z.); ryan.kim2112@gmail.com (H.R.K.); pavel.sumazin@bcm.edu (P.S.) – name: 1 Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, San Diego, CA 92037, USA; fuyu0413@gmail.com (Y.F.); ilorrai@scripps.edu (I.L.); cshankula@scripps.edu (C.S.); jmarquez@scripps.edu (J.M.G.); celinelef@gmail.com (C.L.)
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CitedBy_id	crossref_primary_10_1016_j_peptides_2023_171095 crossref_primary_10_1016_j_bbi_2023_07_021
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Copyright	2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2022 by the authors. 2022
Copyright_xml	– notice: 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2022 by the authors. 2022
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Snippet	Substance use disorder is associated with accelerated disease progression in people with human immunodeficiency virus (HIV; PWH). Problem opioid use, including...
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SubjectTerms	Adaptation AIDS Analgesics, Opioid - adverse effects Animals Catheters Cognitive ability Cognitive Dysfunction - chemically induced Cognitive Dysfunction - complications cognitive impairment Drug abuse Drug dosages Drug use Gene expression Glucocorticoids HIV HIV Infections - complications Human immunodeficiency virus Humans Immune system Inflammation Intubation Kinases Laboratory animals Narcotics Neurodegeneration neuroHIV neuroinflammation Neurotoxicity Opioids Oxycodone Oxycodone - adverse effects Pattern recognition Prefrontal cortex Prescription drugs Rats Rats, Transgenic Self-administration Transcription
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Title	Escalated (Dependent) Oxycodone Self-Administration Is Associated with Cognitive Impairment and Transcriptional Evidence of Neurodegeneration in Human Immunodeficiency Virus (HIV) Transgenic Rats
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