PMC:7463108 / 96888-111927 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7463108","sourcedb":"PMC","sourceid":"7463108","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7463108","text":"Questions Remaining – Future Directions\n\nModeling the Pharmacology of Opioid Self-Administration\nOpiate self-administration as seen with addiction can have different CNS consequences than “steady-state” (e.g., continuous via a pump or time-release drug implant) exposure to the same drug (Kreek 1987, 2001; Kreek et al. 2002), and we predict the pharmacokinetic differences in opiate exposure will markedly impact neuroHIV progression. Differential effects based on “on-off” and “steady-state” drug administration schedules have been reported for the stress-responsive hypothalamic-pituitary-adrenal (HPA) axis, the endogenous opioid system, and the dopamine system (Kreek 1973; Kreek et al. 2002; George et al. 2012). Acute opiate exposure typically activates the HPA axis, corticotropin releasing factor, and peripheral steroidogenesis in a species-dependent manner (Koob and Kreek 2007; Cleck and Blendy 2008). Alternatively, chronic self-administration of short-acting opiates suppresses diurnal cortisol rhythmicity (Facchinetti et al. 1984; Vuong et al. 2010), while opiate withdrawal typically evokes HPA activation (Culpepper-Morgan and Kreek 1997; Kreek 2007; Paris et al. 2020). The daily, repeated bouts of relative withdrawal seen with opiate addiction cause sustained HPA activation, stress (Koob and Kreek 2007; Koob 2020), and immune suppression (Eisenstein 2019). Importantly, maintenance therapy with the long-acting drug methadone achieves steady-dose opiate levels and normalization of the HPA axis (Kreek 1973). Further, it is known that HIV infection significantly alters the HPA axis, due to CNS toxicity and cytokine production (Costa et al. 2000; George and Bhangoo 2013; Chrousos and Zapanti 2014).\nAdditionally, the nature of opiate exposure in the context of neuroHIV needs to be considered as it may induce different outcomes on neurotransmitter metabolism and gene expression. Specifically, the NAc shell demonstrates molecular and structural changes associated with intravenous heroin self-administration (Jacobs et al. 2005). Moreover, earlier studies have reported differential alterations in the turnover rates of various neurotransmitters for active versus passive morphine administration, including dopamine, serotonin, γ-aminobutyric acid (GABA), acetylcholine, aspartate, and glutamate during exposure to morphine (Smith et al. 1982, 1984). The disruptions were noticed specifically in brain regions involved in reinforcement processes, including the NAc, frontal cortex, and striatum, and encompassed increased dopamine and norepinephrine levels and turnover, which are central in opiate reward processes (Smith et al. 1982). Heroin abuse is known to downregulate dopaminergic activity in the NAc and may reflect a compensatory reduction in of dopamine biosynthesis in response to excessive dopaminergic stimulation resulting from chronic opiate exposure (Kish et al. 2001). Additionally, HIV is known to interfere with dopamine neurotransmission (Nath et al. 2000b; Gaskill et al. 2017) causing reductions in presynaptic dopamine terminals and dopamine transport in the striatum (Wang et al. 2004; Chang et al. 2008; Midde et al. 2012, 2015). The decline in dopamine function may exacerbate opioid abuse tendencies and drug-seeking behaviors as the rewarding effects of opioids are discounted by neuroHIV.\n\nOpioid Substitution Therapies and the Role of Selective/Biased Agonism in neuroHIV Pathogenesis\nAlthough morphine, methadone, and buprenorphine all activate MOR, each can impart different signals through MOR, related to the nature and timing of their coupling to Gα, Gβγ, β-arrestin and/or regulators of G protein signaling (RGS), since each downstream effector couples into unique cell functions. Functional selectivity occurs at each opioid receptor type, and for most endogenous opioid peptides at all three receptor types (Gomes et al. 2020). Moreover, opioid receptors can be expressed on a subset of virtually every cell type in the CNS—with second messenger coupling to each opioid receptor type potentially being unique, cell-type specific, and context dependent. Thus, the “pluridimensional” (Galandrin and Bouvier 2006; Kenakin 2011; Costa-Neto et al. 2016) actions of any opiate at MOR are sufficiently complicated that it is not possible to predict whether, e.g., morphine, methadone or buprenorphine, would similarly effect any aspect of neuroHIV pathology without empirical testing. Despite their significant use as medication-assisted therapies for treating opioid addiction, few studies have directly compared commonly used opiate substitution therapies (Bell and Strang 2020), especially in relation to HIV (Khalsa et al. 2006; Choi et al. 2020).\nOpioid substitution therapies significantly reduce the frequency of injection drug use (Kwiatkowski and Booth 2001; Pettes et al. 2010), decrease HIV transmission risk (MacArthur et al. 2012; Platt et al. 2016), and reduce drug-related mortality (Mathers et al. 2013) and the risk of opioid overdose (Volkow et al. 2014). Further, improved ARV outcomes among PWH have been reported with opioid substitution therapies, including the uptake and retention on ARV, medication adherence rates, and viral suppression (Low et al. 2016; Mukandavire et al. 2017). The two main medications used for opioid substitution therapy include methadone, a MOR full agonist, and buprenorphine, a MOR partial agonist and partial antagonist of KOR (Noble and Marie 2018). In comparison to methadone, buprenorphine has been shown to have fewer pharmacodynamic interactions with ARVs and causes less opioid withdrawal symptoms potentially due to its partial agonism on MOR, but also due to its high affinity and long duration of MOR binding (Walsh et al. 1994; McCance-Katz 2005; Whelan and Remski 2012). Further, differential proinflammatory and neurotoxic effects have been noted for various opioid treatments (Boland et al. 2014; Fitting et al. 2014b; Carvallo et al. 2015; Dutta and Roy 2015). In primary astrocytes, agonist-selective actions at MOR and KOR can be clearly demonstrated (Bohn et al. 2000; Belcheva et al. 2003; McLennan et al. 2008; Hahn et al. 2010), and we found that morphine, methadone, and buprenorphine differentially increase ROS and [Ca2+]i alone or following Tat co-exposure (Fitting et al. 2014b). Morphine can enhance HIV-1-induced production of cytokines and specifically chemokines (El-Hage et al. 2008a; Dave 2012; El-Hage et al. 2014), while other opioids including methadone, oxycodone, buprenorphine, and DAMGO can decrease inflammatory function and decrease monocyte migration (Boland et al. 2014; Carvallo et al. 2015; Jaureguiberry-Bravo et al. 2016; Chilunda et al. 2019).\nAs most opiate drugs preferentially act via MOR, a potential explanation for differential interactive effects of opioids in the context of neuroHIV is the phenomenon of selective or “biased agonism”, such that different agonists can trigger distinct signaling events at the same receptor (Hauser et al. 2012). For example, coupling of MOR to Gα, Gβγ, and/or β-arrestin have been noted to differ depending on the MOR agonists involved (McPherson et al. 2010; Thompson et al. 2015; Burgueno et al. 2017). Physiologic outcomes of MOR activation in any cell type are determined by a bias for specific signaling pathways, the initial step of which is activation of G proteins and/or β-arrestin (Williams et al. 2013b; Violin et al. 2014; Suomivuori et al. 2020). The subcellular organization of GPCR signaling transduced by heterotrimeric G proteins and β-arrestin has been recently reviewed in detail (Eichel and von Zastrow 2018).\nIn the context of HIV, it has been shown that selective MOR agonists such as endomorphin-1, but not DAMGO or morphine, significantly increase HIV-1 replication in infected microglia (Peterson et al. 1999). This effect might be due to an apparent bias of endomorphin-1 towards arrestin recruitment and receptor phosphorylation, which was significantly correlated with agonist-induced internalization of MOR (McPherson et al. 2010). It is suggested that ligands that display bias towards G protein-mediated pathways and away from β-arrestin 2 recruitment may have improved therapeutic profiles against the development of tolerance and dependence/addiction (McPherson et al. 2010).\n\nOpioid Effects on Antiretroviral Efficacy within the CNS and Vice Versa\nOpioid misuse has been linked to poor adherence to cART (Jeevanjee et al. 2014). However, adherence to ARV therapy improves after initiation of opioid substitution therapy (Nosyk et al. 2015; Low et al. 2016; Adams et al. 2020). Although better adherence can improve therapeutic outcomes in PWH, little information is currently available on the interaction between opioids or opioid substitution therapies and cART specifically within the CNS.\nThere are several known drug-drug interactions between opioids and ARVs that affect systemic concentrations. The partial opioid agonist, buprenorphine, is metabolized primarily by cytochrome P450 (CYP) 3A4 and 2C8. Both buprenorphine and its active metabolite, norbuprenorphine, are glucuronidated by UDP-glucuronosyltransferase (UGT) 1A1 and then excreted in bile. Several ARVs inhibit or induce these metabolic pathways. However, not all interactions are clinically relevant. The boosted protease inhibitor combination, atazanavir/ritonavir, inhibits CYP 3A4 and UGT 1A1, leading to increases in overall systemic exposure of buprenorphine and norbuprenorphine and also results in symptoms of opioid excess, such as increased sedation and impaired cognition (McCance-Katz et al. 2007). Dose adjustments of buprenorphine are recommended when initiating therapy with atazanavir to avoid symptoms of opioid excess. Methadone is a full opioid substrate with multiple metabolic pathways, including CYP 3A4, 2B6, 2C19, 2C9, and 2D6. Several pharmacokinetic interactions are reported between methadone and protease inhibitors. However, withdrawal symptoms are rare, and therefore, dose adjustments are not recommended (Bruce et al. 2006; Meemken et al. 2015). In contrast, efavirenz and nevirapine induce CYP 3A4, resulting in decreased systemic concentrations of methadone and the development of opioid withdrawal symptoms. To avoid opioid withdrawal, increased methadone dosing is recommended when either efavirenz or nevirapine therapy is initiated (Marzolini et al. 2000; Clarke et al. 2001; Meemken et al. 2015). Oxycodone metabolism is inhibited by lopinavir/ritonavir, increasing oxycodone concentrations as well as the self-reported drug effects (Nieminen et al. 2010; Feng et al. 2017).\nThe pharmacokinetic studies above focused on overall systemic exposure of drugs. Plasma concentrations, however, are not always accurate indicators of tissue exposure. Similarly, CNS drug exposure is often estimated based on drug concentrations within the CSF. However, CSF drug levels may not accurately predict brain concentrations. For many drugs with high efflux activities (e.g., substrates of P-gp), CSF tends to over-predict brain tissue concentrations (Liu et al. 2006; Friden et al. 2009; Kodaira et al. 2011, 2014). This could be due, in part, to differential expression of transporters at the blood-CSF barrier vs. BBB. In a study of the ARV drug amprenavir, concentrations of [14C]-amprenavir in CSF versus brain were 23.3 ± 11.2 and 3.33 ± 0.6 nCi/g, respectively, demonstrating overprediction of brain concentrations by CSF (Polli et al. 1999). These studies illustrate the high likelihood of misinterpreting drug brain penetration when using CSF as the surrogate marker. Therefore, direct measurement of brain tissue concentrations in animal models are likely to be more predictive of the interactive effects of ARVs and opioids on ARV and/or opioid brain exposure.\nA few studies have investigated the impact of opioids and ARV administration on drug concentrations within the brain. One study investigated the impact of 5 d continuous exposure to morphine on ARV brain concentrations (dolutegravir, lamivudine and abacavir) and demonstrated that morphine exposure resulted in regionally specific decreases in the concentrations of select ARV drugs (Leibrand et al. 2019) and, furthermore, that the decreases in ARV concentrations (dolutegravir and abacavir) were likely due to increased efflux by the drug efflux transport protein, P-gp (Leibrand et al. 2019). Morphine alterations in P-gp within the brain could have wide reaching impact on other CNS active drugs.\nHIV preferentially infects microglia and perivascular macrophages within the brain, although BMECs, astrocytes, and pericytes can also be infected (Kramer-Hammerle et al. 2005). Achieving optimal intracellular ARV concentrations are essential to suppress the infection. Few studies have examined whether ARV drugs differentially accumulate within different neural cell types and especially within cells of the neurovascular unit. Although nucleoside reverse transcriptase inhibitors (NRTIs) and non-nucleoside reverse transcriptase inhibitors (NNRTIs) are efficacious in inhibiting viral replication within monocyte-derived macrophages, only a few drugs within each ARV class can effectively inhibit viral replication within astrocytes (Gray et al. 2013), which could be a result of poor intracellular accumulation within astrocytes. In vitro studies have demonstrated darunavir and raltegravir intracellular concentrations to be approximately 100-fold lower (with higher EC50 values) in microglia than in PBMCs (Asahchop et al. 2017).\nAnother study measured intracellular concentrations of dolutegravir, tenofovir and emtricitabine in primary human astrocytes, microglia, pericytes and BMECs (Patel et al. 2019). Intracellular ARV concentrations were typically significantly higher in BMECs than in the other brain cell types. Dolutegravir achieved the highest relative concentrations within each cell type, whereas tenofovir accumulated the least (Patel et al. 2019). Furthermore, 24 h treatment with morphine significantly decreased intracellular accumulation of composite ARV concentrations, but only in astrocytes. In contrast, morphine exposure significantly increased the net accumulation of drugs within BMECs compared to controls. BMECs may sequester ARV drugs as a protective mechanism (Patel et al. 2019).\nUsing experimental data from SIV-infected, morphine-addicted macaques, mathematical modeling suggests that morphine exposure increases the proportion of cells with high susceptibility to SIV infection, at least in part, because of increased co-receptor expression (Vaidya et al. 2016). In addition to promoting a higher steady state viral loads and larger CD4 count declines, the model also predicts that morphine exposure results in the need for more efficacious ARV treatment than would be necessary for animals not exposed to morphine (Vaidya et al. 2016). Although the direct impact of morphine on ARV concentrations was not investigated, the study provides evidence supporting morphine’s negative impact on ARV 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