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Metabolic Risk/Epidemiology
Effect of Low-Dose Persistent Organic Pollutants on Mitochondrial Function: Human and in Vitro Evidence
Se-A Kim, Hoyul Lee, Sung-Mi Park, Mi-Jin Kim, Yu-Mi Lee, Young-Ran Yoon, Hyun-Kyung Lee, Hyo-Bang Moon, In-Kyu Lee, Duk-Hee Lee
Diabetes Metab J. 2022;46(4):592-604.   Published online January 26, 2022
DOI: https://doi.org/10.4093/dmj.2021.0132
  • 5,972 View
  • 251 Download
  • 7 Web of Science
  • 9 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   ePub   
Background
Chronic exposure to low-dose persistent organic pollutants (POPs) can induce mitochondrial dysfunction. This study evaluated the association between serum POP concentrations and oxygen consumption rate (OCR) as a marker of mitochondrial function in humans and in vitro cells.
Methods
Serum concentrations of organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) were measured in 323 adults. The OCRs of platelets and peripheral blood mononuclear cells (PBMCs) were assessed in 20 mL of fresh blood using a Seahorse XF analyzer. Additionally, the in vitro effects of Arochlor-1254, β-hexachlorocyclohexane, and p,p´-dichlorodiphenyltrichloroethane at concentrations of 0.1 pM to 100 nM were evaluated in human platelets, human PBMCs, and Jurkat T-cells.
Results
The association between serum POP concentrations and OCR differed depending on the cell type. As serum OCP concentrations increased, basal platelet OCR levels decreased significantly; according to the OCP quintiles of summary measure, they were 8.6, 9.6, 8.2, 8.0, and 7.1 pmol/min/μg (P trend=0.005). Notably, the basal PBMC OCR levels decreased remarkably as the serum PCB concentration increased. PBMC OCR levels were 46.5, 34.3, 29.1, 16.5, and 13.1 pmol/min/μg according to the PCB quintiles of summary measure (P trend <0.001), and this inverse association was consistently observed in all subgroups stratified by age, sex, obesity, type 2 diabetes mellitus, and hypertension, respectively. In vitro experimental studies have also demonstrated that chronic exposure to low-dose POPs could decrease OCR levels.
Conclusion
The findings from human and in vitro studies suggest that chronic exposure to low-dose POPs can induce mitochondrial dysfunction by impairing oxidative phosphorylation.

Citations

Citations to this article as recorded by  
  • Persistent Organic Pollutants released from decomposed adipose tissue affect mitochondrial enzyme function in the brain and eyes other than the liver
    Dongshin Yang, Eun Ko, Hwayeon Lim, Hyojin Lee, Kitae Kim, Moonsung Choi, Sooim Shin
    Environmental Science and Pollution Research.2024;[Epub]     CrossRef
  • Obesity paradox can be a fact: unveiling the hidden role of adipose tissue
    Duk-Hee Lee
    European Heart Journal.2024; 45(24): 2167.     CrossRef
  • Reduced bioenergetics and mitochondrial fragmentation in human primary cytotrophoblasts induced by an EGFR-targeting chemical mixture
    Anita A. Waye, Elvis Ticiani, Zinat Sharmin, Vanessa Perez Silos, Thilini Perera, Alex Tu, Irina A. Buhimschi, Carlos A. Murga-Zamalloa, Ying S. Hu, Almudena Veiga-Lopez
    Chemosphere.2024; 364: 143301.     CrossRef
  • Can lipophilic pollutants in adipose tissue explain weight change‐related risk in type 2 diabetes mellitus?
    Duk‐Hee Lee, In‐Kyu Lee
    Journal of Diabetes Investigation.2023; 14(4): 528.     CrossRef
  • Mitochondrial and metabolic features of salugenesis and the healing cycle
    Robert K. Naviaux
    Mitochondrion.2023; 70: 131.     CrossRef
  • Obesity Paradox in Sepsis: Role of Adipose Tissue in Storing Mitochondrial Toxins
    Duk-Hee Lee
    Critical Care Medicine.2023; 51(8): e172.     CrossRef
  • Human Preadipocytes Differentiated under Hypoxia following PCB126 Exposure during Proliferation: Effects on Differentiation, Glucose Uptake and Adipokine Profile
    Zeinab El Amine, Jean-François Mauger, Pascal Imbeault
    Cells.2023; 12(18): 2326.     CrossRef
  • Is micronucleus assay in oral exfoliated cells a useful biomarker for biomonitoring populations exposed to pesticides? A systematic review with meta-analysis
    Ingra Tais Malacarne, Wilton Mitsunari Takeshita, Daniel Vitor de Souza, Barbara dos Anjos Rosario, Milena de Barros Viana, Ana Claudia Muniz Renno, Daisy Maria Favero Salvadori, Daniel Araki Ribeiro
    Environmental Science and Pollution Research.2022; 29(43): 64392.     CrossRef
  • Comment on: Obesity is Associated with Improved Postoperative Overall Survival, Independent of Skeletal Muscle Mass in Lung Adenocarcinoma by Lee et al.
    Duk‐Hee Lee
    Journal of Cachexia, Sarcopenia and Muscle.2022; 13(5): 2576.     CrossRef
Others
Article image
Can Habitual Exercise Help Reduce Serum Concentrations of Lipophilic Chemical Mixtures? Association between Physical Activity and Persistent Organic Pollutants
Yu-Mi Lee, Ji-Yeon Shin, Se-A Kim, David R. Jacobs, Duk-Hee Lee
Diabetes Metab J. 2020;44(5):764-774.   Published online May 11, 2020
DOI: https://doi.org/10.4093/dmj.2019.0158
  • 6,020 View
  • 91 Download
  • 8 Web of Science
  • 11 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   ePub   
Background

Low-dose persistent organic pollutants (POPs), especially organochlorine pesticides (OCPs), have emerged as a new risk factor of many chronic diseases. As serum concentrations of POPs in humans are mainly determined by both their release from adipose tissue to circulation and their elimination from circulation, management of these internal pathways may be important in controlling the serum concentrations of POPs. As habitual physical activity can increase the elimination of POPs from circulation, we evaluated whether chronic physical activity is related to low serum POP concentrations.

Methods

A cross-sectional study of 1,850 healthy adults (age ≥20 years) without cardio-metabolic diseases who participated in the U.S. National Health and Nutrition Examination Survey 1999 to 2004 was conducted. Information on moderate or vigorous leisure-time physical activity was obtained based on questionnaires. Serum concentrations of OCPs and polychlorinated biphenyls were investigated as typical POPs.

Results

Serum concentrations of OCPs among physically active subjects were significantly lower than those among physically inactive subjects (312.8 ng/g lipid vs. 538.0 ng/g lipid, P<0.001). This difference was maintained after adjustment for potential confounders. When analyses were restricted to physically active subjects, there were small decreases in the serum concentrations of OCPs with increasing duration of physical activity, showing a curvilinear relationship over the whole range of physical activity (Pquadratic <0.001). In analyses stratified by age, sex, body mass index, and smoking status, a strong inverse association was similarly observed among all subgroups.

Conclusion

Physical activity may assist in decreasing serum concentrations of lipophilic chemical mixtures such as OCPs.

Citations

Citations to this article as recorded by  
  • Is Physical Activity an Efficient Strategy to Control the Adverse Effects of Persistent Organic Pollutants in the Context of Obesity? A Narrative Review
    Quentin A. Serrano, Sébastien Le Garf, Vincent Martin, Serge S. Colson, Nicolas Chevalier
    International Journal of Molecular Sciences.2024; 25(2): 883.     CrossRef
  • Untargeted metabolomics reveal signatures of a healthy lifestyle
    Wimal Pathmasiri, Blake R. Rushing, Susan McRitchie, Mansi Choudhari, Xiuxia Du, Alexsandr Smirnov, Matteo Pelleigrini, Michael J. Thompson, Camila A. Sakaguchi, David C. Nieman, Susan J. Sumner
    Scientific Reports.2024;[Epub]     CrossRef
  • Unraveling the pesticide-diabetes connection: A case-cohort study integrating Mendelian randomization analysis with a focus on physical activity's mitigating effect
    Dandan Wei, Jiayu Shi, Zhiwei Chen, Haoran Xu, Xuyan Wu, Yao Guo, Xin Zen, Caini Fan, Xiaotian Liu, Jian Hou, Wenqian Huo, Linlin Li, Tao Jing, Chongjian Wang, Zhenxing Mao
    Ecotoxicology and Environmental Safety.2024; 283: 116778.     CrossRef
  • Prospective study on the joint effect of persistent organic pollutants and glucose metabolism on chronic kidney disease: Modifying effects of lifestyle interventions
    Dandan Wei, Jiayu Shi, Haoran Xu, Yao Guo, Xueyan Wu, Zhiwei Chen, Taimeng Chen, Huilin Lou, Erbao Han, Guozhen Han, Yumeng Yan, Xiaotian Liu, Xin Zeng, Caini Fan, Jian Hou, Wenqian Huo, Linlin Li, Tao Jing, Chongjian Wang, Zhenxing Mao
    Science of The Total Environment.2024; 951: 175694.     CrossRef
  • Associations between polychlorinated biphenyls and cancer risk among type 2 diabetes: The modifying effects of lifestyle
    Peiwen Li, Yu Wang, Qianying Liu, Yan Yan, Zhuoya Zhao, Shiyang Zhang, Chengyong Jia, Jun An, Cheng Xu, Xin Zhang, Tao Jing, Huan Guo, Meian He
    Chemosphere.2024; 366: 143442.     CrossRef
  • Physical exercise and persistent organic pollutants
    Chang Liu, Hui sheng Hou
    Heliyon.2023; 9(9): e19661.     CrossRef
  • Exposure to a low concentration of mixed organochlorine pesticides impairs glucose metabolism and mitochondrial function in L6 myotubes and zebrafish
    Chul-Min Park, Ki-Tae Kim, Dong-Young Rhyu
    Journal of Hazardous Materials.2021; 414: 125437.     CrossRef
  • Can Environmental Pollutants Be a Factor Linking Obesity and COVID-19?
    Duk-Hee Lee
    Journal of Korean Medical Science.2021;[Epub]     CrossRef
  • Letter to the Editor: Effect of fatty fish or nut consumption on concentrations of persistent organic pollutants in overweight or obese men and women: A randomized controlled clinical trial
    Yu-Mi Lee, Duk-Hee Lee
    Nutrition, Metabolism and Cardiovascular Diseases.2020; 30(5): 849.     CrossRef
  • Can habitual exercise really increase serum concentrations of persistent organic pollutants?
    Yu-Mi Lee, Duk-Hee Lee
    Environment International.2020; 140: 105615.     CrossRef
  • Response to correspondence ENVINT_2020_552 “Can habitual exercise really increase serum concentrations of persistent organic pollutants?”
    Sidsel L. Domazet, Tina K. Jensen, Anders Grøntved
    Environment International.2020; 140: 105616.     CrossRef

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