Mitochondrial oxidative phosphorylation in peripheral blood mononuclear cells is decreased in chronic HIV and correlates with immune dysregulation

Cellular immunometabolism among people living with HIV (PLWH) on antiretroviral therapy (ART) remains under investigated. We assessed the relationships between mitochondrial oxidative phosphorylation (OXPHOS) in peripheral blood mononuclear cells (PBMCs) and blood parameters associated with HIV immu...

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Published in:PloS one 2020-04, Vol.15 (4), p.e0231761
Main Authors: Gangcuangco, Louie Mar A, Mitchell, Brooks I, Siriwardhana, Chathura, Kohorn, Lindsay B, Chew, Glen M, Bowler, Scott, Kallianpur, Kalpana J, Chow, Dominic C, Ndhlovu, Lishomwa C, Gerschenson, Mariana, Shikuma, Cecilia M
Format: Article
Language:English
Subjects:
Adenosine triphosphate
Age
Anti-HIV Agents - therapeutic use
Antiretroviral agents
Antiretroviral therapy
Biology and Life Sciences
Blood
CD14 antigen
CD16 antigen
CD4 antigen
CD4-CD8 Ratio
CD8 antigen
Cell activation
Chronic fatigue syndrome
Cross-Sectional Studies
Cytochrome
Cytochrome-c oxidase
Cytochromes
Dehydrogenases
Deoxyribonucleic acid
Didanosine
Disease
DNA
Enzymes
Exhaustion
Female
Flow cytometry
Hawaii
HIV
HIV Infections - diagnosis
HIV Infections - drug therapy
HIV Infections - immunology
HIV Infections - virology
HIV-1 - genetics
HIV-1 - immunology
HIV-1 - isolation & purification
Host-Pathogen Interactions - immunology
Human immunodeficiency virus
Humans
Immunoassay
Immunoassays
Inflammation
Leukocytes (mononuclear)
Leukocytes, Mononuclear - cytology
Leukocytes, Mononuclear - immunology
Level (quantity)
Lymphocyte Activation
Lymphocytes T
Male
Medicine and Health Sciences
Middle Aged
Minority & ethnic groups
Mitochondria
Mitochondria - immunology
Mitochondria - metabolism
Mitochondrial DNA
Monocytes
Mutation
NADH
NADH dehydrogenase
Nicotinamide adenine dinucleotide
Optical density
Oxidative Phosphorylation
Peripheral blood mononuclear cells
Phosphorylation
Protein X
Proteins
Respiration
Ribonucleic acid
RNA
RNA, Viral - isolation & purification
Senescence
Severity of Illness Index
Zidovudine
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container_issue 4
container_start_page e0231761
container_title PloS one
container_volume 15
creator Gangcuangco, Louie Mar A
Mitchell, Brooks I
Siriwardhana, Chathura
Kohorn, Lindsay B
Chew, Glen M
Bowler, Scott
Kallianpur, Kalpana J
Chow, Dominic C
Ndhlovu, Lishomwa C
Gerschenson, Mariana
Shikuma, Cecilia M
description Cellular immunometabolism among people living with HIV (PLWH) on antiretroviral therapy (ART) remains under investigated. We assessed the relationships between mitochondrial oxidative phosphorylation (OXPHOS) in peripheral blood mononuclear cells (PBMCs) and blood parameters associated with HIV immune dysregulation. PLWH ≥40 years old and on stable ART ≥3 months were enrolled (N = 149). OXPHOS complex I (CI, NADH dehydrogenase) and complex IV (CIV, cytochrome c oxidase) protein levels in PBMCs were quantified using immunoassays. Monocyte subsets and markers of T-cell activation, senescence, and exhaustion were measured on PBMC by flow cytometry. Plasma inflammatory mediators were quantified using a multiplex assay. HIV-uninfected group (N = 44) of similar age, gender, and ethnicity had available OXPHOS levels. PLWH had a median age of 51 years. Majority were male (88.6%), Caucasian (57.7%), and with undetectable plasma HIV RNA
doi_str_mv 10.1371/journal.pone.0231761
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We assessed the relationships between mitochondrial oxidative phosphorylation (OXPHOS) in peripheral blood mononuclear cells (PBMCs) and blood parameters associated with HIV immune dysregulation. PLWH ≥40 years old and on stable ART ≥3 months were enrolled (N = 149). OXPHOS complex I (CI, NADH dehydrogenase) and complex IV (CIV, cytochrome c oxidase) protein levels in PBMCs were quantified using immunoassays. Monocyte subsets and markers of T-cell activation, senescence, and exhaustion were measured on PBMC by flow cytometry. Plasma inflammatory mediators were quantified using a multiplex assay. HIV-uninfected group (N = 44) of similar age, gender, and ethnicity had available OXPHOS levels. PLWH had a median age of 51 years. Majority were male (88.6%), Caucasian (57.7%), and with undetectable plasma HIV RNA &lt;50 copies/mL (84.6%). Median CI level was lower in PLWH compared with the HIV-seronegative group (65.5 vs 155.0 optical density/μg protein x 103, p &lt;0.0001). There was no significant difference in median CIV levels. Lower OXPHOS levels correlated with lower CD4% and CD4/CD8 ratio. On multivariable linear regression adjusted for age, current use of zidovudine/didanosine, and HIV RNA (detectable versus undetectable), lower OXPHOS levels were significantly associated with higher MPO, SAA, SAP, and sVCAM, and higher frequencies of intermediate (CD14++CD16+) monocytes and TIGIT+TIM3+ CD4 T-cell (p&lt;0.01). CI PBMC protein levels were decreased in PLWH on ART. Decreased OXPHOS correlated with disease severity and inflammation. 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Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agriculture Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials science collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gangcuangco, Louie Mar A</au><au>Mitchell, Brooks I</au><au>Siriwardhana, Chathura</au><au>Kohorn, Lindsay B</au><au>Chew, Glen M</au><au>Bowler, Scott</au><au>Kallianpur, Kalpana J</au><au>Chow, Dominic C</au><au>Ndhlovu, Lishomwa C</au><au>Gerschenson, Mariana</au><au>Shikuma, Cecilia M</au><au>Yu, Qigui</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mitochondrial oxidative phosphorylation in peripheral blood mononuclear cells is decreased in chronic HIV and correlates with immune dysregulation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-04-30</date><risdate>2020</risdate><volume>15</volume><issue>4</issue><spage>e0231761</spage><pages>e0231761-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Cellular immunometabolism among people living with HIV (PLWH) on antiretroviral therapy (ART) remains under investigated. We assessed the relationships between mitochondrial oxidative phosphorylation (OXPHOS) in peripheral blood mononuclear cells (PBMCs) and blood parameters associated with HIV immune dysregulation. PLWH ≥40 years old and on stable ART ≥3 months were enrolled (N = 149). OXPHOS complex I (CI, NADH dehydrogenase) and complex IV (CIV, cytochrome c oxidase) protein levels in PBMCs were quantified using immunoassays. Monocyte subsets and markers of T-cell activation, senescence, and exhaustion were measured on PBMC by flow cytometry. Plasma inflammatory mediators were quantified using a multiplex assay. HIV-uninfected group (N = 44) of similar age, gender, and ethnicity had available OXPHOS levels. PLWH had a median age of 51 years. Majority were male (88.6%), Caucasian (57.7%), and with undetectable plasma HIV RNA &lt;50 copies/mL (84.6%). Median CI level was lower in PLWH compared with the HIV-seronegative group (65.5 vs 155.0 optical density/μg protein x 103, p &lt;0.0001). There was no significant difference in median CIV levels. Lower OXPHOS levels correlated with lower CD4% and CD4/CD8 ratio. On multivariable linear regression adjusted for age, current use of zidovudine/didanosine, and HIV RNA (detectable versus undetectable), lower OXPHOS levels were significantly associated with higher MPO, SAA, SAP, and sVCAM, and higher frequencies of intermediate (CD14++CD16+) monocytes and TIGIT+TIM3+ CD4 T-cell (p&lt;0.01). CI PBMC protein levels were decreased in PLWH on ART. Decreased OXPHOS correlated with disease severity and inflammation. Further studies on the relationship between immunometabolism and immune dysregulation in HIV are warranted.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32353005</pmid><doi>10.1371/journal.pone.0231761</doi><orcidid>https://orcid.org/0000-0001-8881-6941</orcidid><orcidid>https://orcid.org/0000-0002-6714-9294</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
ispartof PloS one, 2020-04, Vol.15 (4), p.e0231761
issn 1932-6203
1932-6203
language eng
recordid cdi_plos_journals_2396928030
source Publicly Available Content Database; PubMed Central
subjects Adenosine triphosphate
Age
Anti-HIV Agents - therapeutic use
Antiretroviral agents
Antiretroviral therapy
Biology and Life Sciences
Blood
CD14 antigen
CD16 antigen
CD4 antigen
CD4-CD8 Ratio
CD8 antigen
Cell activation
Chronic fatigue syndrome
Cross-Sectional Studies
Cytochrome
Cytochrome-c oxidase
Cytochromes
Dehydrogenases
Deoxyribonucleic acid
Didanosine
Disease
DNA
Enzymes
Exhaustion
Female
Flow cytometry
Hawaii
HIV
HIV Infections - diagnosis
HIV Infections - drug therapy
HIV Infections - immunology
HIV Infections - virology
HIV-1 - genetics
HIV-1 - immunology
HIV-1 - isolation & purification
Host-Pathogen Interactions - immunology
Human immunodeficiency virus
Humans
Immunoassay
Immunoassays
Inflammation
Leukocytes (mononuclear)
Leukocytes, Mononuclear - cytology
Leukocytes, Mononuclear - immunology
Level (quantity)
Lymphocyte Activation
Lymphocytes T
Male
Medicine and Health Sciences
Middle Aged
Minority & ethnic groups
Mitochondria
Mitochondria - immunology
Mitochondria - metabolism
Mitochondrial DNA
Monocytes
Mutation
NADH
NADH dehydrogenase
Nicotinamide adenine dinucleotide
Optical density
Oxidative Phosphorylation
Peripheral blood mononuclear cells
Phosphorylation
Protein X
Proteins
Respiration
Ribonucleic acid
RNA
RNA, Viral - isolation & purification
Senescence
Severity of Illness Index
Zidovudine
title Mitochondrial oxidative phosphorylation in peripheral blood mononuclear cells is decreased in chronic HIV and correlates with immune dysregulation
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