Chronic cannabis smoking-enriched oral pathobiont drives behavioral changes, macrophage infiltration, and increases β-amyloid protein production in the brain.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Dec 2021
Historique:
received: 10 08 2021
revised: 24 10 2021
accepted: 03 11 2021
pubmed: 27 11 2021
medline: 22 3 2022
entrez: 26 11 2021
Statut: ppublish

Résumé

Little is known about chronic cannabis smoking-associated oral microbiome and its effects on central nervous system (CNS) functions. In the current study, we have analyzed the saliva microbiome in individuals who chronically smoked cannabis with cannabis use disorder (n = 16) and in non-smoking controls (n = 27). The saliva microbiome was analyzed using microbial 16S rRNA sequencing. To investigate the function of cannabis use-associated oral microbiome, mice were orally inoculated with live Actinomyces meyeri, Actinomyces odontolyticus, or Neisseria elongata twice per week for six months, which mimicked human conditions. We found that cannabis smoking in humans was associated with oral microbial dysbiosis. The most increased oral bacteria were Streptococcus and Actinomyces genus and the most decreased bacteria were Neisseria genus in chronic cannabis smokers compared to those in non-smokers. Among the distinct species bacteria in cannabis smokers, the enrichment of Actinomyces meyeri was inversely associated with the age of first cannabis smoking. Strikingly, oral exposure of Actinomyces meyeri, an oral pathobiont, but not the other two control bacteria, decreased global activity, increased macrophage infiltration, and increased β-amyloid 42 protein production in the mouse brains. This is the first study to reveal that long-term oral cannabis exposure is associated oral enrichment of Actinomyces meyeri and its contributions to CNS abnormalities.

Sections du résumé

BACKGROUND BACKGROUND
Little is known about chronic cannabis smoking-associated oral microbiome and its effects on central nervous system (CNS) functions.
METHODS METHODS
In the current study, we have analyzed the saliva microbiome in individuals who chronically smoked cannabis with cannabis use disorder (n = 16) and in non-smoking controls (n = 27). The saliva microbiome was analyzed using microbial 16S rRNA sequencing. To investigate the function of cannabis use-associated oral microbiome, mice were orally inoculated with live Actinomyces meyeri, Actinomyces odontolyticus, or Neisseria elongata twice per week for six months, which mimicked human conditions.
FINDINGS RESULTS
We found that cannabis smoking in humans was associated with oral microbial dysbiosis. The most increased oral bacteria were Streptococcus and Actinomyces genus and the most decreased bacteria were Neisseria genus in chronic cannabis smokers compared to those in non-smokers. Among the distinct species bacteria in cannabis smokers, the enrichment of Actinomyces meyeri was inversely associated with the age of first cannabis smoking. Strikingly, oral exposure of Actinomyces meyeri, an oral pathobiont, but not the other two control bacteria, decreased global activity, increased macrophage infiltration, and increased β-amyloid 42 protein production in the mouse brains.
INTERPRETATION CONCLUSIONS
This is the first study to reveal that long-term oral cannabis exposure is associated oral enrichment of Actinomyces meyeri and its contributions to CNS abnormalities.

Identifiants

pubmed: 34826801
pii: S2352-3964(21)00495-3
doi: 10.1016/j.ebiom.2021.103701
pmc: PMC8626580
pii:
doi:

Substances chimiques

Amyloid beta-Peptides 0
DNA, Bacterial 0
DNA, Ribosomal 0
RNA, Ribosomal, 16S 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

103701

Subventions

Organisme : NIA NIH HHS
ID : R21 AG074331
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD096501
Pays : United States
Organisme : NIDA NIH HHS
ID : K24 DA038240
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG054159
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA045596
Pays : United States
Organisme : NIA NIH HHS
ID : K23 AG044434
Pays : United States
Organisme : NIGMS NIH HHS
ID : U54 GM104941
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS099595
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001450
Pays : United States
Organisme : NINR NIH HHS
ID : P20 NR016605
Pays : United States
Organisme : NIAMS NIH HHS
ID : P30 AR072582
Pays : United States
Organisme : NIGMS NIH HHS
ID : P20 GM109040
Pays : United States
Organisme : NINR NIH HHS
ID : R01 NR016928
Pays : United States

Informations de copyright

Copyright © 2021. Published by Elsevier B.V.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare no competing interests.

Auteurs

Zhenwu Luo (Z)

Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Ave., Charleston, SC 29425, USA.

Sylvia Fitting (S)

Department of Psychology and Neuroscience, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.

Catrina Robinson (C)

Department of Neurology, Medical University of South Carolina, Charleston, SC 29425, USA.

Andreana Benitez (A)

Department of Neurology, Medical University of South Carolina, Charleston, SC 29425, USA.

Min Li (M)

Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Ave., Charleston, SC 29425, USA.

Yongxia Wu (Y)

Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Ave., Charleston, SC 29425, USA.

Xiaoyu Fu (X)

Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Ave., Charleston, SC 29425, USA; Department of Infectious Disease, Key Laboratory of Hunan Viral Hepatitis, Xiangya Hospital, Central South University, Changsha, Hunan 410008, China.

Davide Amato (D)

Department of Neurosciences, Medical University of South Carolina, Charleston, SC 29425, USA.

Wangbin Ning (W)

Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Ave., Charleston, SC 29425, USA; Department of Rheumatology and Immunology, Xiangya Hospital, Central South University, Changsha, Hunan 410008, China.

Nicholas Funderburg (N)

Division of Medical Laboratory Science, School of Health and Rehabilitation Sciences, Ohio State University College of Medicine, Columbus, OH, USA.

Xu Wang (X)

Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Ave., Charleston, SC 29425, USA; Department of Urology, Capital Medical University Affiliated XuanWu Hospital, 45 Changchun Street, Xicheng District, Beijing 100053, China.

Zejun Zhou (Z)

State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal University, Changsha 410081, China.

Xuezhong Yu (X)

Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Ave., Charleston, SC 29425, USA.

Amanda Wagner (A)

Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, SC 29425, USA.

Xiaomei Cong (X)

Department of Pediatrics, School of Medicine, School of Nursing, Institute for Systems Genomics, University of Connecticut, Storrs, CT, USA.

Wanli Xu (W)

Department of Pediatrics, School of Medicine, School of Nursing, Institute for Systems Genomics, University of Connecticut, Storrs, CT, USA.

Kendra Maas (K)

Microbial Analysis, Resources, and Services, University of Connecticut, Storrs, CT, USA.

Bethany J Wolf (BJ)

Department of Public Health Sciences, Medical University of South Carolina, Charleston, SC 29425, USA.

Lei Huang (L)

Treatment and Research Center for Infectious Diseases, The Fifth Medical Center of Chinese PLA General Hospital, Beijing, China.

Jeremy Yu (J)

Department of Medicine, Division of Endocrinology, Diabetes and Metabolic Diseases, Medical University of South Carolina, Charleston, SC 29425, USA.

Alison Scott (A)

Department of Microbial Pathogenesis, School of Dentistry, University of Maryland, Baltimore, MD 21201, USA.

Aimee Mcrae-Clark (A)

Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, SC 29425, USA.

Eric D Hamlett (ED)

Department of Pathology and Laboratory Medicine, Medical University of South Carolina, Charleston, SC 29425, USA. Electronic address: hamlette@musc.edu.

Wei Jiang (W)

Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Ave., Charleston, SC 29425, USA; Department of Medicine, Division of Infectious Diseases, Medical University of South Carolina, Charleston, SC 29425, USA. Electronic address: jianw@musc.edu.

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Classifications MeSH