PMC:7463108 / 41057-47302 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":"Opioid and HIV Interactive Pathology in Astroglia\nAlthough the extent to which astroglia display productive infection is debated (Russell et al. 2017; Ko et al. 2019), there is nevertheless considerable evidence of proviral integration in the CNS of PWH (Gorry et al. 2003; Churchill et al. 2009), infectious animal models (Eugenin et al. 2011), and/or cultured human fetal astrocytes (Tornatore et al. 1994; Liu et al. 2004; Do et al. 2014; Narasipura et al. 2014; Li et al. 2015; Nath 2015; Li et al. 2020). Integrated HIV sequences have been identified in astrocytes in HIV-infected CNS tissue by laser capture microdissection (Churchill et al. 2006). Astroglia appear to infect via non-classical, CD4-independent mechanisms, that can have the appearance of virologic synapses, adding to the debate (Liu et al. 2004; Do et al. 2014; Li et al. 2015; Nath 2015; Al-Harthi et al. 2019; Li et al. 2020).\nIrrespective of whether they become infected, MOR-expressing, HIV or HIV protein-exposed astrocytes release greater amounts of inflammatory cytokines and dysfunction sufficient to harm bystander neurons upon treatment with opiates (El-Hage et al. 2005, 2008b; Zou et al. 2011; El-Hage et al. 2014). MOR-expressing subsets of glia, especially microglia and astroglia, are prominent in driving the interactive opioid and HIV neuropathogenesis (Hauser et al. 2007, 2012; Hauser and Knapp 2014; Liu et al. 2016a; Chilunda et al. 2019; Murphy et al. 2019). When MOR is deleted from glia (astrocytes and microglia), morphine no longer increases the death of Tat-exposed striatal medium spiny neurons (MSNs) (Zou et al. 2011). Conversely, if MOR is deleted from MSNs, morphine exacerbates the neurotoxic effects of Tat in MSNs (Zou et al. 2011). The proinflammatory effects of Tat alone or in combination with morphine on glia are mediated through a Beclin-1-dependent autophagy pathway (Rodriguez et al. 2017; Lapierre et al. 2018). Drugs with selective glial anti-inflammatory activity (i.e., ibudilast or AV411) attenuated the deleterious effects of HIV and opiate exposure, including HIV-1 replication, cytokine release, and neurotoxicity in vitro (El-Hage et al. 2014). Thus, the observed neuronal death is largely mediated by MOR-expressing glia (Zou et al. 2011), including astroglia (El-Hage et al. 2005, 2008b) and microglia (Turchan-Cholewo et al. 2008; Bokhari et al. 2009; Turchan-Cholewo et al. 2009; Gupta et al. 2010).\nThe direct contributions of astrocytes to opioid and HIV interactions have been discussed previously (Dutta and Roy 2012; Hauser et al. 2012; Reddy et al. 2012; Hauser and Knapp 2014). Subsets of astroglia can express MOR, DOR and KOR (Stiene-Martin and Hauser 1991; Eriksson et al. 1992; Ruzicka et al. 1995; Gurwell et al. 1996; Hauser et al. 1996; Peterson et al. 1998; Stiene-Martin et al. 1998, 2001), as well as endogenous opioid peptides (Vilijn et al. 1988; Shinoda et al. 1989; Spruce et al. 1990; Hauser et al. 1990; Low et al. 1992). It appears that the ‘early’ events triggering the release of proinflammatory cytokines (i.e., TNF-α and IL-1β) from astroglia can be mediated by HIV Tat exposure alone (El-Hage et al. 2005, 2006a, b, 2008a). Opioids enhance HIV-1-induced inflammation later during the inflammatory cascade by exacerbating the sustained release of CCL5 from astrocytes, which subsequently triggers the release of CCL2 thereby enhancing the recruitment and activation of macrophages/microglia (El-Hage et al. 2008a) (Fig. 1). This is caused by the morphine-dependent exacerbation of Tat-induced increases in intracellular calcium concentration ([Ca2+]i) in astroglia (El-Hage et al. 2005), which accelerates the trafficking of NF-κB p65 (RelA) subunits to the nucleus and sustained CCL2, CCL5, and IL-6 transcription in astrocytes (El-Hage et al. 2008b).\nFig. 1 Opioids exacerbate HIV-1-induced CNS inflammation, in part, by augmenting CCL5-dependent increases in CCL2—key sites of opioid-HIV convergent interactions in glial inflammatory signaling cascades. Subpopulations of striatal glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in wildtype mice normally express CCR2 immunoreactivity (a-b; arrows), CCL2 (c; arrow), or μ-opioid receptor (MOR) (d; arrows) immunoreactivity (scale bars a-b = 25 μm; c-d = 15 μm). CCR2 deletion (−/−) significantly reduces HIV-1 Tat ± morphine-induced increases in GFAP+ astroglia (e) and F4/80+ macrophages/microglia (f) compared to wild type (+/+) mice at sites near (300 ± 100 μm) the site of Tat injection (*p \u003c 0.05 vs. wild type mice) (see, El-Hage et al. 2006a). In wild-type mice, Tat ± morphine administration markedly increases the proportion of CCL2 immunoreactive astrocytes (g) or macrophages/microglia (h) [*p \u003c 0.05 vs. other groups in wild-type or CCL5(−/−) mice; bp \u003c 0.05 vs. vehicle- or Tat plus morphine-treated wild-type mice; #p \u003c 0.05 vs. equivalent treatment in wild-type mice], while in CCL5 null mice, significant increases in CCL2 immunoreactivity were only seen in macrophages/microglia co-exposed to Tat and morphine (§p \u003c 0.05 vs. vehicle injected CCL5 knockout mice) (see, El-Hage et al. 2008a). CCL5 expression in striatal GFAP-immunoreactive astrocytes (arrows) increases following Tat injections (i, j) compared to wild-type control mice (not shown) (El-Hage et al. 2008a). Opioids exacerbate HIV-1-induced CNS inflammation, in part, by increasing CCL5 and augmenting CCR5-dependent increases in CCL2 production by astrocytes resulting in the activation and recruitment of microglia/macrophages and spiraling inflammation (k). Additional factors likely mediate the proinflammatory cascade, but these are less well substantiated (?). Moreover, autocrine and reciprocal paracrine (astroglial ↔ macrophage/microglial) intercellular, feedback amplification mechanisms from macrophages/microglia are likely to be operative (dashed red arrow) (also see, Kang and Hebert 2011) and occur elsewhere within the cascade (not shown); effects of HIV-1 Tat/HIV, red arrows; sites of opioid convergence, blue arrows; pro-BDNF:mature BDNF (mBDNF) ratio (Kim et al. 2018). (a-f) Modified and reprinted with permission from El-Hage et al. (2006a). (g-k) Modified and reprinted with permission from El-Hage et al. 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