PM2.5 induce lifespan reduction, insulin/IGF-1 signaling pathway disruption and lipid metabolism disorder in Caenorhabditis elegans

Wenjing Zhang; Zinan Li; Guojun Li; Ling Kong; Haiming Jing; Nan Zhang; Junyu Ning; Shan Gao; Yong Zhang; Xinyu Wang; Jing Tao

doi:10.3389/fpubh.2023.1055175

PM_2.5 induce lifespan reduction, insulin/IGF-1 signaling pathway disruption and lipid metabolism disorder in Caenorhabditis elegans

Front Public Health. 2023 Feb 2:11:1055175. doi: 10.3389/fpubh.2023.1055175. eCollection 2023.

Authors

Wenjing Zhang¹, Zinan Li^{1

2}, Guojun Li^{1

2}, Ling Kong¹, Haiming Jing^{1

2}, Nan Zhang¹, Junyu Ning^{1

2}, Shan Gao¹, Yong Zhang¹, Xinyu Wang¹, Jing Tao¹

Affiliations

¹ Beijing Center for Disease Prevention and Control, Beijing, China.
² School of Public Health, Capital Medical University, Beijing, China.

Abstract

Introduction: Exposure to fine particulate matter (PM), especially PM_2.5, can induce various adverse health effects in populations, including diseases and premature death, but the mechanism of its toxicity is largely unknown.

Methods: Water-soluble components of PM_2.5 (WS-PM_2.5) were collected in the north of China in winter, and combined in two groups with the final concentrations of 94 μg/mL (C_L group, AQI ≤ 100) and 119 μg/mL (C_H group, 100 < AQI ≤ 200), respectively. The acute and long-term toxic effects of WS-PM_2.5 samples were evaluated in several aspects such as development, lifespan, healthspan (locomotion behavior, heat stress tolerance, lipofucin). DAF mutants and genes were applied to verify the action of IIS pathway in WS-PM_2.5 induced-effects. RNA-Sequencing was performed to elucidate the molecular mechanisms, as well as ROS production and Oil red O staining were also served as means of mechanism exploration.

Results: Body length and lifespan were shortened by exposure to WS-PM_2.5. Healthspan of nematodes revealed adverse effects evaluated by head thrash, body bend, pharyngeal pump, as well as intestinal lipofuscin accumulation and survival time under heat stress. The abbreviated lifespan of daf-2(e1370) strain and reduced expression level of daf-16 and hsp-16.2 indicated that IIS pathway might be involved in the mechanism. Thirty-five abnormally expressed genes screened out by RNA-Sequencing techniques, were functionally enriched in lipid/lipid metabolism and transport, and may contribute substantially to the regulation of PM_2.5 induced adverse effects in nematodes.

Conclusion: WS-PM_2.5 exposure induce varying degrees of toxic effects, such as body development, shorten lifespan and healthspan. The IIS pathway and lipid metabolism/transport were disturbed by WS-PM_2.5 during WS-PM_2.5 exposure, suggesting their regulatory role in lifespan determination.

Keywords: Caenorhabditis elegans; PM2.5; RNA-Sequencing; gene homology; healthspan; lifespan.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Caenorhabditis elegans* / genetics
Caenorhabditis elegans* / metabolism
Insulin / metabolism
Insulin / pharmacology
Insulin-Like Growth Factor I / genetics
Insulin-Like Growth Factor I / metabolism
Lipid Metabolism
Lipid Metabolism Disorders*
Longevity / genetics
Particulate Matter / toxicity
RNA / metabolism
RNA / pharmacology
Signal Transduction

Substances

Insulin
Particulate Matter
Insulin-Like Growth Factor I
RNA

Grants and funding

This work was supported by National Natural Science Foundation of China (Grant Nos: 81273108, 81641184), The Capital Health Research and Development of Special Fund in Beijing (Grant No: 2011-1013-03). The funders had no role in the study design, data collection, and analysis, decision to publish, or preparation of the manuscript.