Role of Brain Derived Extracellular Vesicles in Decoding Sex Differences Associated with Nicotine Self-Administration

Koul, Sneh; Schaal, Victoria L.; Chand, Subhash; Pittenger, Steven T.; Vellichirammal, Neetha Nanoth; Kumar, Vikas; Guda, Chittibabu; Bevins, Rick A.; Yelamanchili, Sowmya V.; Pendyala, Gurudutt

doi:10.3390/cells9081883

Cited by 11 publications

(21 citation statements)

References 85 publications

(118 reference statements)

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“…In males, 6 proteins were upregulated and 79 were downregulated. Overall, this study found sex-specific alterations in BDEV biogenesis and cargo content following nicotine self-administration [131].…”

Section: Nicotinesupporting

confidence: 53%

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Role of Extracellular Vesicles in Substance Abuse and HIV-Related Neurological Pathologies

Odegaard

Chand

Wheeler

et al. 2020

IJMS

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Extracellular vesicles (EVs) are a broad, heterogeneous class of membranous lipid-bilayer vesicles that facilitate intercellular communication throughout the body. As important carriers of various types of cargo, including proteins, lipids, DNA fragments, and a variety of small noncoding RNAs, including miRNAs, mRNAs, and siRNAs, EVs may play an important role in the development of addiction and other neurological pathologies, particularly those related to HIV. In this review, we summarize the findings of EV studies in the context of methamphetamine (METH), cocaine, nicotine, opioid, and alcohol use disorders, highlighting important EV cargoes that may contribute to addiction. Additionally, as HIV and substance abuse are often comorbid, we discuss the potential role of EVs in the intersection of substance abuse and HIV. Taken together, the studies presented in this comprehensive review shed light on the potential role of EVs in the exacerbation of substance use and HIV. As a subject of growing interest, EVs may continue to provide information about mechanisms and pathogenesis in substance use disorders and CNS pathologies, perhaps allowing for exploration into potential therapeutic options.

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Section: Nicotinesupporting

confidence: 53%

“…Nicotine use has recently been shown to have a sex-specific effect pattern on brain-derived EVs (BDEVs) [131]. In a rat self-administration paradigm of nicotine, females had larger BDEV sizes and impaired EV biogenesis compared to males following nicotine self-administration.…”

Section: Nicotinementioning

confidence: 99%

Role of Extracellular Vesicles in Substance Abuse and HIV-Related Neurological Pathologies

Odegaard

Chand

Wheeler

et al. 2020

IJMS

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“…Several studies have undertaken analyses of nicotine-induced alterations in the brain proteome. These studies include investigations of whole brain tissue (Miller et al, 2018;Paulo et al, 2018;Koul et al, 2020) or specific brain regions, including hippocampus (Matsuura et al, 2016;Zhu et al, 2017), cortex (Matsuura et al, 2016;Hwang and Li, 2006;McClure-Begley et al, 2016), amygdala (Hwang and Li, 2006), dorsal striatum (Petruzziello et al, 2013;Hishimoto et al, 2016;Hwang and Li, 2006;Yeom et al, 2005), NAc, and VTA (Hwang and Li, 2006) in mice and rats. Nicotine administration ranged from an acute injection 48 hours prior to tissue collection (Hishimoto et al, 2016) to 6 months of nicotine administration through drinking water (Matsuura et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…Despite evidence for 1 https://www.who.int/news-room/fact-sheets/detail/tobacco significant sex differences in nicotine addiction, 7 of the 10 studies published to date used only male animal subjects, one study only female animal subjects, and one study did not report the sex of its animal subjects. Only one study used both male and female animal subjects and specifically focused on the proteomic signatures of brain-derived extracellular vesicles in their analysis of sex differences after long-term nicotine self-administration (Koul et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Sex Differences in the Ventral Tegmental Area and Nucleus Accumbens Proteome at Baseline and Following Nicotine Exposure

Lee

Mansuri²,

Wilson³

et al. 2021

Front. Mol. Neurosci.

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Sex differences in behaviors relevant to nicotine addiction have been observed in rodent models and human subjects. Behavioral, imaging, and epidemiological studies also suggest underlying sex differences in mesolimbic dopamine signaling pathways. In this study we evaluated the proteome in the ventral tegmental area (VTA) and nucleus accumbens (NAc) shell in male and female mice. Experimental groups included two mouse strains (C3H/HeJ and C57BL/6J) at baseline, a sub-chronic, rewarding regimen of nicotine in C3H/HeJ mice, and chronic nicotine administration and withdrawal in C57BL/6J mice. Isobaric labeling with a TMT 10-plex system, sample fractionation, and tandem mass spectrometry were used to quantify changes in protein abundance. In C3H/HeJ mice, similar numbers of proteins were differentially regulated between sexes at baseline compared with within each sex after sub-chronic nicotine administration. In C57BL/6J mice, there were significantly greater numbers of proteins differentially regulated between sexes at baseline compared with within each sex after chronic nicotine administration and withdrawal. Despite differences by sex, strain, and nicotine exposure parameters, glial fibrillary acidic protein (GFAP) and dopamine and cAMP-regulated phosphoprotein of 32 kDa (DARPP-32, Ppp1r1b) were repeatedly identified as significantly altered proteins, especially in the VTA. Further, network analyses showed sex- and nicotine-dependent regulation of a number of signaling pathways, including dopaminergic signaling. Sub-chronic nicotine exposure in female mice increased proteins related to dopaminergic signaling in the NAc shell but decreased them in the VTA, whereas the opposite pattern was observed in male mice. In contrast, dopaminergic signaling pathways were similarly upregulated in both male and female VTA after chronic nicotine and withdrawal. Overall, this study identifies significant sex differences in the proteome of the mesolimbic system, at baseline and after nicotine reward or withdrawal, which may help explain differential trajectories and susceptibility to nicotine addiction in males and females.

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“…For example, sex‐specific changes in brain‐derived extracellular vesicles biogenesis and protein cargo signatures have been identified in rats post nicotine self‐administration. 74 The synovial fluid extracellular vesicle protein content is altered in a sex‐specific manner with osteoarthritis 75 which explains the increased prevalence and severity of osteoarthritis in women. In stroke research, sex differences also have been found at cellular levels 76 and the whole animal.…”

Section: The Roles Of Exs In Cns Injury Diseasesmentioning

confidence: 99%

The promise of exosome applications in treating central nervous system diseases

Mattingly

Bihl

et al. 2021

CNS Neurosci Ther

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Exosomes (EXs) are a major type of extracellular vesicles released by cells highly conserved from microorganisms to mammals. 1 Their size ranges from 20 to 150 nm in diameter. About 50 years ago, they were initially considered cellular "waste." In the early 1980s, EXs were recognized as distinct entities. Later in 1987, the term "exosome" was coined for these membrane particles. Over the past decades, increasing evidence shows that EXs can cross the blood-brain barrier (BBB) and serve cell-to-cell communicators via conveying their carried biological cargoes (nuclear acids, proteins, and lipids). 2,3 In the central nervous system (CNS), EXs are released from virtually all brain cells, including neurons, astrocytes, microglia, and endothelial cells., 4,5 and exchange molecule messages related to neuronal function and neurotransmission in the brain via the reciprocal communication between brain cells.Given the capability of EXs to reach body compartments and connect origin cells with target cells, EXs have a promising potential to be used in clinical applications. Indeed, a large body of preclinical studies has shown the implication and therapeutic potential of EXs in CNS diseases. Here, we review the current state of the knowledge of EXs, the roles and applications of EXs as a viable pathological biomarker, and EX-based therapy for CNS diseases. | OVERVIE W OF E X S | EX biogenesis, isolation, and contentsEX generation is initiated by a process that involves double invagination of the plasma membrane and the formation of intracellular multivesicular bodies (MVBs). The MVBs contain intraluminal vesicles that are secreted as EXs via exocytosis and MVB fusion to the plasma membrane. 6,7 Although the exact biogenesis mechanism has not been fully delineated, multiple molecules including Ras-related

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Role of Brain Derived Extracellular Vesicles in Decoding Sex Differences Associated with Nicotine Self-Administration

Cited by 11 publications

References 85 publications

Role of Extracellular Vesicles in Substance Abuse and HIV-Related Neurological Pathologies

Role of Extracellular Vesicles in Substance Abuse and HIV-Related Neurological Pathologies

Sex Differences in the Ventral Tegmental Area and Nucleus Accumbens Proteome at Baseline and Following Nicotine Exposure

The promise of exosome applications in treating central nervous system diseases

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