PMC:7463108 / 80608-92834 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":"MOR and Chemokine Receptor Interactions (CCR5, CXCR4)\nThe ability of opiates to modulate HIV infection and HIV neuropathogenesis/disease progression may be partly due to the interactive effects seen between the opioid and chemokine receptors, specifically MOR and CCR5 or CXCR4 (Rogers and Peterson 2003; Steele et al. 2003; Szabo et al. 2003; Festa and Meucci 2012). The potential mechanisms for this interaction can include heterologous cross-desensitization via downstream signaling (Rogers et al. 2000; Steele et al. 2002; Song et al. 2011) and/or potentially via direct opioid-chemokine receptor dimeric or heteromeric interactions (Suzuki et al. 2002; Chen et al. 2004; Nash and Meucci 2014). MOR and DOR activation can heterologously desensitize CCR5 responsiveness to CCL3, CCL4, and CCL5 in monocytes (Grimm et al. 1998; Szabo et al. 2003; Chen et al. 2004). The cross-desensitization appears to be regulated by MOR-dependent PKCζ activation and CCR5 phosphorylation and downregulation (Song et al. 2011). Alternatively, MOR-induced downregulation of CCL2 and CCL4 mRNA reciprocally upregulates the expression of their associated receptors, CCR2b, CCR3, and CCR5 (Mahajan et al. 2005). A previous study reported significant upregulation of CCR5 and CXCR4 expression in CD14 monocytes with [D-Ala2, N-MePhe4, Gly-ol]-enkephalin (DAMGO), a MOR ligand, exposure with enhanced replication of both X4- and R5-tropic viral strains of HIV (Steele et al. 2003). For CXCR4, bidirectional heterologous desensitization is less evident with MOR but has been reported for KOR, with Ca2+ signaling experiments suggesting that cross-desensitization occurs within seconds of KOR or CXCR4 activation in a concentration-dependent manner (Finley et al. 2008). Thus, opiates acting at different opioid receptors in the presence of HIV appear to activate chemokine receptor signaling and can contribute to the synergistic effects of HIV and opioid drug co-exposure seen in neuroHIV progression.\nThe ability of opiates to modulate CCR5 expression in the CNS has been demonstrated to occur in various cell types, including microglia (Bokhari et al. 2009), and astrocytes (Mahajan et al. 2002). Specifically, in astrocytes MOR activation enhanced CCR5 and additional HIV-1 entry co-receptor (CCR3 and CXCR2) expression, whereas local production of HIV-1 protective chemokines (IL-8, CCL4) was inhibited (Mahajan et al. 2002). Deletion of CCR5 significantly attenuates morphine-induced increases in astrocyte CCL2 immunoreactivity in Tat transgenic mice (El-Hage et al. 2008a) (Fig. 1). Interestingly, the proportion of CCL2 immunoreactive macrophages/microglia in CCL5(−/−) mice after Tat and morphine co-administration still showed a significant upregulation, suggesting CCL5 regulates Tat and morphine-induced increases in CCL2 in astrocytes, but not in microglia (El-Hage et al. 2008a) (Fig. 1).\nThe cell type specific interactions between CCR5 and MOR were noted when using a bivalent ligand derivative of maraviroc linked to an opioid antagonist, naltrexone, with HIV-1 entry being significantly blocked in astrocytes but not microglia (El-Hage et al. 2013) (Fig. 5). Interestingly, maraviroc’s antiviral effects are completely negated in both astrocytes and microglia when morphine is present suggesting that maraviroc therapy may not be effective with opiate co-exposure. Importantly, unlike maraviroc, the bivalent compound blocked HIV entry in astrocytes irrespective of morphine treatment, while exacerbating HIV infectivity in morphine co-exposed microglia and revealing fundamental differences in the regulation of MOR and CCR5 expression in these glial types. Whereas, MOR and CCR5 expression appear to be similarly regulated in astrocytes, their expression patterns in microglia appear to be inversely correlated upon HIV and/or morphine exposure, with CCR5 being expressed at much higher levels than MOR (see El-Hage et al. 2013). The differential effects of the bivalent ligand in astrocytes compared to microglia might be due to the fact that the expression levels of MOR and CCR5 are differentially regulated by HIV in each of the cell types (El-Hage et al. 2013; Yuan et al. 2013; Arnatt et al. 2016).\nFig. 5 Differential inhibition of HIV-1 entry into human glia by maraviroc and a bivalent CCR5-MOR antagonist (BVL) with cell-specific interactions in combination with morphine. (a) Construction of a MOR-CCR5 heterodimer model in a membrane (gray), and aqueous surrounds (red) system. The green protein represents MOR and the blue protein represents CCR5, while the bivalent ligand is colored in yellow. (b) Different binding pocket (green) for the triazole moiety of the bivalent ligand yellow) at 0 ns and 6.0 ns. (c) Construction of a chemical probe that interacts with both the MOR and CCR5 receptors simultaneously. To monitor HIV-1 infection (d) astrocytes and (e) microglia were transfected with a pBlue3′LTR-luc reporter sensitive to Tat expression and luciferase activity was measured. Data indicate that maraviroc’s antiviral effects are completely negated in both astrocytes and microglia when morphine is present (red bars). Interestingly, unlike maraviroc, the bivalent compound blocked HIV entry in astrocytes irrespective of morphine treatment. By contrast, the bivalent antagonist exacerbated HIV infectivity in microglia in the presence of morphine (red bars). The findings reveal fundamental differences in co-regulation of MOR and CCR5 expression in astroglia and microglia upon HIV and/or morphine exposure (see El-Hage et al. 2013). Values are luminescence intensity ± SEM from 3 to 5 independent experiments at 18 h post-infection (*p \u003c 0.005 vs. un-infected cells; $p \u003c 0.05 vs. R5 HIV-1; #p \u003c 0.05 vs. R5 + morphine (M); ¶p \u003c 0.05 vs. R5 + maraviroc (MVC); §p \u003c 0.05 vs. R5 + M + MVC; ¥p \u003c 0.05 vs. R5 + M + MVC + naltrexone). (a–b) Modified and reprinted with permission from Arnatt et al. (2016). (c–e) Modified and reprinted with permission from El-Hage et al. (2013)\nThe importance of CCR5 activation in glia, but not neurons, in mediating the neurotoxic effects of morphine-dependent MOR activation is further supported in a recent study demonstrating that the loss of CCR5 from glia (but not neurons) eliminated neurotoxicity due to Tat and morphine interactions (Kim et al. 2018). Similarly, short-duration (5 d) maraviroc pre-treatment also eliminated neurotoxicity and attenuated neuronal increases in [Ca2+]i caused by Tat ± morphine (Kim et al. 2018). Selectively deleting either CCR5 (Kim et al. 2018) or MOR (Zou et al. 2011) from glia completely protects MSNs from morphine’s ability to exacerbate Tat neurotoxicity. However, deleting CCR5 from glia only revealed a paradoxical neuroprotective effect of morphine on Tat toxicity that is mediated by opioid receptors and appears to involve alterations in BDNF processing and signaling (Kim et al. 2018).\n\nEnhanced Mature BDNF (mBDNF) Produced by CCR5 Deficient Glia is Neuroprotective\nMature BDNF (mBDNF) activates tyrosine receptor kinase B (TrkB) and is neuroprotective, while the precursor to BDNF, pro-BDNF, binds p75NTR and can activate cell death pathways. Based on findings of significant, reversible reductions in glially produced BDNF after exposure to HIV-infected cell supernatant ± morphine (Masvekar et al. 2014), altered BDNF processing in lymphocytes from PWH (Avdoshina et al. 2011), and following exposure to HIV-1 gp120 (Bachis et al. 2012), the pro-BDNF:mBDNF ratio was analyzed in supernatants from wild-type vs. CCR5-null striatal glial cultures exposed to Tat ± morphine for 6 or 24 h (Kim et al. 2018) (Fig. 6). CCR5-deficiency reduced this ratio by over 2-fold in cells treated with Tat and morphine after 6 h (Fig. 6), indicating a relative increase in mBDNF that may partially protect neurons in the CCR5-deficient glial environment.\nFig. 6 Role of CCR5 and BDNF in mediating HIV-1 Tat and morphine-induced interactive cytotoxicity in striatal medium spiny neurons (MSNs). A proportion of glial fibrillary acidic protein (GFAP)-immunolabeled striatal astrocytes display punctate patterns of μ-opioid receptor (MOR) (a) and CCR5 (b) (43.8 ± 2.4%) immunofluorescence—with some faint immunoreactivity extending into the cell processes; scale bars = 10 μm (a-b). HIV-1 Tat and morphine are no longer toxic to MSNs when CCR5 is deleted from glia (c-f). In C57BL/J wild-type mixed glia-MSN co-cultures, Tat is neurotoxic (*p = 0.001 vs. controls), and co-exposure to morphine enhanced Tat-induced toxicity over a 72-h period (**p \u003c 0.001 vs. controls, p \u003c 0.05 vs. Tat) and antagonized by naloxone (c). Naloxone or morphine by themselves had no effect on neuronal survival (c). In co-cultures with CCR5-deficit glia and wild-type neurons, exposure to Tat by itself is significantly toxic (*p \u003c 0.001 vs. controls); however, the enhanced toxicity seen with combined morphine exposure was eliminated (d). Unexpectedly, morphine co-treatment entirely abolished the toxic effects of Tat, restoring MSN survival to control levels. Pre-treatment with naloxone re-established Tat toxicity, suggesting that the paradoxical protective effects of morphine are mediated by MOR (or perhaps another opioid receptor type) (d) (see Kim et al. 2018). The neurotoxic patterns seen in CCR5-deficient MSNs and wild-type glial co-cultures are similar to wild-type co-cultures (e). Co-cultures in which MSNs and glia are both deficient in CCR5 are similar to those in which CCR5 is only deficient in glia (f). CCR5 deletion alters the expression and processing of BDNF precursor (pro-BDNF) to mature (mBDNF) by mixed-glial cultures (g). BDNF is expressed by both astroglia and microglia; mBDNF is neuroprotective, while pro-BDNF can promote programmed cell death. mBDNF and pro-BDNF levels were analyzed in conditioned media from wild-type or CCR5-deficient mixed glia treated with Tat ± morphine after 6 h or 24 h to assess pro-BDNF and mBDNF levels. The proportion of pro-BDNF/mBDNF levels was significantly higher in wild-type compared to CCR5-null glia at 24 h (lower row; g), suggesting reduced neuronal support. Although morphine significantly decreased pro-BDNF in CCR5-deficient glia at both 6 h and 24 h compared to control levels (not shown), the pro-BDNF/mBDNF ratios were unaltered (upper and lower rows; g). By contrast, combined Tat and morphine significantly decreased the pro-BDNF/mBDNF ratio at 6 h, suggesting transient protection with CCR5 deficiency that was not fully sustained at 24 h (p = 0.17) (*p \u003c 0.05, wild-type vs. CCR5-null) (g). Exogenous mBDNF is neuroprotective against combined Tat and morphine treatment (h). Wild-type, mixed glial-MSN co-cultures were treated with mBDNF and Tat, or combined Tat and morphine (represented by dotted survival curves). Tat alone was neurotoxic (*p \u003c 0.05), and Tat was significantly worsened by co-exposing MSNs to morphine (**p \u003c 0.0001). The addition of mBDNF (50 ng/ml; 72 h) fully protected MSNs against combined Tat and morphine toxicity, but only tended to protect (albeit not significantly) MSNs treated with Tat alone (#)(h). Overall, the results in c-h suggest (1) an important role for glial CCR5 in mediating HIV-1 and opiate neurotoxic interactions, (2) that CCR5 deficiency influences signaling through MOR, and (3) that CCR5 (and perhaps MOR) act via a BDNF intermediary to promote or obstruct neuronal survival (Kim et al. 2018). (a-b) Modified and reprinted with permission from Podhaizer et al. (2012). (c-h) Modified and reprinted from Kim et al. (2018), which is an open access article distributed under the terms of the Creative Commons CC BY license\nExogenous mBDNF treatment has been found to mimic the pro-survival effect of glial CCR5 deficiency against Tat ± morphine, and its neuroprotective effects have been supported in other neurodegenerative disease models (Cai et al. 2014; Xu et al. 2018). Collectively, the findings suggest that the loss of CCR5 may fundamentally change MOR signaling in HIV-exposed glia in a BDNF-dependent manner. Thus, overall the interaction of opioid and chemokine receptors, specifically MOR and CCR5, may alter the neuropathogenesis of HIV in a qualitatively unique manner not seen with either disorder 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