A comprehensive study to delineate the role of an extracellular vesicle‐associated microRNA‐29a in chronic methamphetamine use disorder

Extracellular vesicles (EVs), which express a repertoire of cargo molecules (cf. proteins, microRNA, lipids, etc.), have been garnering a prominent role in the modulation of several cellular processes. Here, using both non‐human primate and rodent model systems, we provide evidence that brain‐derive...

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Published inJournal of extracellular vesicles Vol. 10; no. 14; pp. e12177 - n/a
Main Authors Chand, Subhash, Gowen, Austin, Savine, Mason, Moore, Dalia, Clark, Alexander, Huynh, Wendy, Wu, Niming, Odegaard, Katherine, Weyrich, Lucas, Bevins, Rick A., Fox, Howard S., Pendyala, Gurudutt, Yelamanchili, Sowmya V.
Format Journal Article
LanguageEnglish
Published United States John Wiley & Sons, Inc 01.12.2021
John Wiley and Sons Inc
Wiley
Subjects
Abstinence
Animals
Biomarkers
Biosynthesis
Brain
Chronic Disease
Cytokines
Extracellular vesicles
Extracellular Vesicles - metabolism
Humans
Inflammation
Lipids
Macaca mulatta
Methamphetamine
Methamphetamine - adverse effects
MicroRNAs
MicroRNAs - adverse effects
miRNA
Pathogenesis
Reinstatement
Tumor necrosis factor-TNF
Online AccessGet full text
ISSN2001-3078
2001-3078
DOI10.1002/jev2.12177

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Abstract Extracellular vesicles (EVs), which express a repertoire of cargo molecules (cf. proteins, microRNA, lipids, etc.), have been garnering a prominent role in the modulation of several cellular processes. Here, using both non‐human primate and rodent model systems, we provide evidence that brain‐derived EV (BDE) miRNA, miR‐29a‐3p (mir‐29a), is significantly increased during chronic methamphetamine (MA) exposure. Further, miR‐29a levels show significant increase both with drug‐seeking and reinstatement in a rat MA self‐administration model. We also show that EV‐associated miR‐29a is enriched in EV pool comprising of small EVs and exomeres and further plays a critical role in MA‐induced inflammation and synaptodendritic damage. Furthermore, treatment with the anti‐inflammatory drug ibudilast (AV411), which is known to reduce MA relapse, decreased the expression of miR‐29a and subsequently attenuated inflammation and rescued synaptodendritic injury. Finally, using plasma from MUD subjects, we provide translational evidence that EV‐miR29a could potentially serve as a biomarker to detect neuronal damage in humans diagnosed with MA use disorder (MUD). In summary, our work suggests that EV‐associated miR‐29a‐3p plays a crucial role in MUD and might be used as a potential blood‐based biomarker for detecting chronic inflammation and synaptic damage.
AbstractList Extracellular vesicles (EVs), which express a repertoire of cargo molecules (cf. proteins, microRNA, lipids, etc.), have been garnering a prominent role in the modulation of several cellular processes. Here, using both non‐human primate and rodent model systems, we provide evidence that brain‐derived EV (BDE) miRNA, miR‐29a‐3p (mir‐29a), is significantly increased during chronic methamphetamine (MA) exposure. Further, miR‐29a levels show significant increase both with drug‐seeking and reinstatement in a rat MA self‐administration model. We also show that EV‐associated miR‐29a is enriched in EV pool comprising of small EVs and exomeres and further plays a critical role in MA‐induced inflammation and synaptodendritic damage. Furthermore, treatment with the anti‐inflammatory drug ibudilast (AV411), which is known to reduce MA relapse, decreased the expression of miR‐29a and subsequently attenuated inflammation and rescued synaptodendritic injury. Finally, using plasma from MUD subjects, we provide translational evidence that EV‐miR29a could potentially serve as a biomarker to detect neuronal damage in humans diagnosed with MA use disorder (MUD). In summary, our work suggests that EV‐associated miR‐29a‐3p plays a crucial role in MUD and might be used as a potential blood‐based biomarker for detecting chronic inflammation and synaptic damage.
Extracellular vesicles (EVs), which express a repertoire of cargo molecules (cf. proteins, microRNA, lipids, etc.), have been garnering a prominent role in the modulation of several cellular processes. Here, using both non-human primate and rodent model systems, we provide evidence that brain-derived EV (BDE) miRNA, miR-29a-3p (mir-29a), is significantly increased during chronic methamphetamine (MA) exposure. Further, miR-29a levels show significant increase both with drug-seeking and reinstatement in a rat MA self-administration model. We also show that EV-associated miR-29a is enriched in EV pool comprising of small EVs and exomeres and further plays a critical role in MA-induced inflammation and synaptodendritic damage. Furthermore, treatment with the anti-inflammatory drug ibudilast (AV411), which is known to reduce MA relapse, decreased the expression of miR-29a and subsequently attenuated inflammation and rescued synaptodendritic injury. Finally, using plasma from MUD subjects, we provide translational evidence that EV-miR29a could potentially serve as a biomarker to detect neuronal damage in humans diagnosed with MA use disorder (MUD). In summary, our work suggests that EV-associated miR-29a-3p plays a crucial role in MUD and might be used as a potential blood-based biomarker for detecting chronic inflammation and synaptic damage.Extracellular vesicles (EVs), which express a repertoire of cargo molecules (cf. proteins, microRNA, lipids, etc.), have been garnering a prominent role in the modulation of several cellular processes. Here, using both non-human primate and rodent model systems, we provide evidence that brain-derived EV (BDE) miRNA, miR-29a-3p (mir-29a), is significantly increased during chronic methamphetamine (MA) exposure. Further, miR-29a levels show significant increase both with drug-seeking and reinstatement in a rat MA self-administration model. We also show that EV-associated miR-29a is enriched in EV pool comprising of small EVs and exomeres and further plays a critical role in MA-induced inflammation and synaptodendritic damage. Furthermore, treatment with the anti-inflammatory drug ibudilast (AV411), which is known to reduce MA relapse, decreased the expression of miR-29a and subsequently attenuated inflammation and rescued synaptodendritic injury. Finally, using plasma from MUD subjects, we provide translational evidence that EV-miR29a could potentially serve as a biomarker to detect neuronal damage in humans diagnosed with MA use disorder (MUD). In summary, our work suggests that EV-associated miR-29a-3p plays a crucial role in MUD and might be used as a potential blood-based biomarker for detecting chronic inflammation and synaptic damage.
Abstract Extracellular vesicles (EVs), which express a repertoire of cargo molecules (cf. proteins, microRNA, lipids, etc.), have been garnering a prominent role in the modulation of several cellular processes. Here, using both non‐human primate and rodent model systems, we provide evidence that brain‐derived EV (BDE) miRNA, miR‐29a‐3p (mir‐29a), is significantly increased during chronic methamphetamine (MA) exposure. Further, miR‐29a levels show significant increase both with drug‐seeking and reinstatement in a rat MA self‐administration model. We also show that EV‐associated miR‐29a is enriched in EV pool comprising of small EVs and exomeres and further plays a critical role in MA‐induced inflammation and synaptodendritic damage. Furthermore, treatment with the anti‐inflammatory drug ibudilast (AV411), which is known to reduce MA relapse, decreased the expression of miR‐29a and subsequently attenuated inflammation and rescued synaptodendritic injury. Finally, using plasma from MUD subjects, we provide translational evidence that EV‐miR29a could potentially serve as a biomarker to detect neuronal damage in humans diagnosed with MA use disorder (MUD). In summary, our work suggests that EV‐associated miR‐29a‐3p plays a crucial role in MUD and might be used as a potential blood‐based biomarker for detecting chronic inflammation and synaptic damage.
Author Clark, Alexander
Huynh, Wendy
Moore, Dalia
Fox, Howard S.
Pendyala, Gurudutt
Wu, Niming
Bevins, Rick A.
Weyrich, Lucas
Odegaard, Katherine
Savine, Mason
Gowen, Austin
Chand, Subhash
Yelamanchili, Sowmya V.
AuthorAffiliation 2 Department of Psychology University of Nebraska–Lincoln (UNL) Lincoln Nebraska USA
4 Midland University Omaha Nebraska USA
3 Department of Pharmacology and Experimental Neuroscience University of Nebraska Medical Center (UNMC) Omaha Nebraska USA
5 Department of Neurological Sciences University of Nebraska Medical Center (UNMC) Omaha Nebraska USA
1 Department of Anesthesiology University of Nebraska Medical Center (UNMC) Omaha Nebraska USA
AuthorAffiliation_xml – name: 4 Midland University Omaha Nebraska USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/34913274$$D View this record in MEDLINE/PubMed
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Notes Subhash Chand and Austin Gowen contributed equally to this work.
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wiley_primary_10_1002_jev2_12177_JEV212177
ProviderPackageCode CITATION
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PublicationCentury 2000
PublicationDate December 2021
2021-12-00
20211201
2021-12-01
PublicationDateYYYYMMDD 2021-12-01
PublicationDate_xml – month: 12
  year: 2021
  text: December 2021
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: Abingdon
– name: Hoboken
PublicationTitle Journal of extracellular vesicles
PublicationTitleAlternate J Extracell Vesicles
PublicationYear 2021
Publisher John Wiley & Sons, Inc
John Wiley and Sons Inc
Wiley
Publisher_xml – name: John Wiley & Sons, Inc
– name: John Wiley and Sons Inc
– name: Wiley
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Snippet Extracellular vesicles (EVs), which express a repertoire of cargo molecules (cf. proteins, microRNA, lipids, etc.), have been garnering a prominent role in the...
Abstract Extracellular vesicles (EVs), which express a repertoire of cargo molecules (cf. proteins, microRNA, lipids, etc.), have been garnering a prominent...
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StartPage e12177
SubjectTerms Abstinence
Animals
Biomarkers
Biosynthesis
Brain
Chronic Disease
Cytokines
Extracellular vesicles
Extracellular Vesicles - metabolism
Humans
Inflammation
Lipids
Macaca mulatta
Methamphetamine
Methamphetamine - adverse effects
MicroRNAs
MicroRNAs - adverse effects
miRNA
Pathogenesis
Reinstatement
Tumor necrosis factor-TNF
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Title A comprehensive study to delineate the role of an extracellular vesicle‐associated microRNA‐29a in chronic methamphetamine use disorder
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