Enhanced Intrusion of Exogenous Airborne Fine Particles Toward Eyes in Humans and Animals: Where Damaged Blood-Ocular Barrier Plays a Crucial Role

Overview

Journal Environ Sci Technol

Publisher American Chemical Society

Specialty Environmental Health

Date 2024 Jul 4

PMID 38961559

Authors

Yu Qi

Xiaoxue Liu

Yucai Chen

Yue Wu

Yu Sun

Xiaoyu Liu

Qingdong Bao

Jingjing Zhang

Gongqiang Yuan

Ting Wang

Xiaolei Sun

Sijin Liu

Hua Gao

Affiliations

Soon will be listed here.

Abstract

Emerging data suggest a close correlation between ambient fine particle (AFP) exposure and eye disorders and pinpoint potential threats of AFPs to eye health in humans. However, the possible passage (including direct intrusion) and the interactions of AFPs with the eye microenvironment in addition to morphological and physiological injuries remain elusive. To this end, the likely transport of AFPs into the eyes via blood-ocular barrier (BOB) in humans and animals was investigated herein. Exogenous particles were recognized inside human eyes with detailed structural and chemical fingerprints. Importantly, comparable AFPs were found in sera with constant structural and chemical fingerprints, hinting at the translocation pathway from blood circulation into the eye. Furthermore, we found that the particle concentrations in human eyes from patients with diabetic retinopathy were much higher than those from patients with no fundus pathological changes (i.e., myopia), indicating that the damaged BOB increased the possibility of particle entrance. Our diseased animal model further corroborated these findings. Collectively, our results offer a new piece of evidence on the intrusion of exogenous particles into human eyes and provide an explanation for AFP-induced eye disorders, with substantially increased risk in susceptible individuals with BOB injuries.

References

Chen W, Lu X, Yuan D, Chen Y, Li Z, Huang Y . Global PM Prediction and Associated Mortality to 2100 under Different Climate Change Scenarios. Environ Sci Technol. 2023; 57(27):10039-10052. DOI: 10.1021/acs.est.3c03804. View

Yuan T, Zou H . Effects of air pollution on myopia: an update on clinical evidence and biological mechanisms. Environ Sci Pollut Res Int. 2022; 29(47):70674-70685. PMC: 9515022. DOI: 10.1007/s11356-022-22764-9. View

Kiel J, Hollingsworth M, Rao R, Chen M, Reitsamer H . Ciliary blood flow and aqueous humor production. Prog Retin Eye Res. 2010; 30(1):1-17. PMC: 3010334. DOI: 10.1016/j.preteyeres.2010.08.001. View

Qi Y, Chen Y, Yan X, Liu W, Ma L, Liu Y . Co-Exposure of Ambient Particulate Matter and Airborne Transmission Pathogens: The Impairment of the Upper Respiratory Systems. Environ Sci Technol. 2022; 56(22):15892-15901. PMC: 9670849. DOI: 10.1021/acs.est.2c03856. View

Lin Y, Li Y, Amesho K, Shangdiar S, Chou F, Cheng P . Chemical characterization of PM emissions and atmospheric metallic element concentrations in PM emitted from mobile source gasoline-fueled vehicles. Sci Total Environ. 2020; 739:139942. DOI: 10.1016/j.scitotenv.2020.139942. View

Bove H, Bongaerts E, Slenders E, Bijnens E, Saenen N, Gyselaers W . Ambient black carbon particles reach the fetal side of human placenta. Nat Commun. 2019; 10(1):3866. PMC: 6748955. DOI: 10.1038/s41467-019-11654-3. View

Wheeler K, Chetwynd A, Fahy K, Hong B, Tochihuitl J, Foster L . Environmental dimensions of the protein corona. Nat Nanotechnol. 2021; 16(6):617-629. DOI: 10.1038/s41565-021-00924-1. View

Qi Y, Chen Y, Xia T, Lynch I, Liu S . Extra-Pulmonary Translocation of Exogenous Ambient Nanoparticles in the Human Body. ACS Nano. 2022; 17(1):12-19. PMC: 9835979. DOI: 10.1021/acsnano.2c09299. View

Bobo D, Robinson K, Islam J, Thurecht K, Corrie S . Nanoparticle-Based Medicines: A Review of FDA-Approved Materials and Clinical Trials to Date. Pharm Res. 2016; 33(10):2373-87. DOI: 10.1007/s11095-016-1958-5. View

10.

Gu Y, Hao S, Liu K, Gao M, Lu B, Sheng F . Airborne fine particulate matter (PM) damages the inner blood-retinal barrier by inducing inflammation and ferroptosis in retinal vascular endothelial cells. Sci Total Environ. 2022; 838(Pt 4):156563. DOI: 10.1016/j.scitotenv.2022.156563. View

11.

Jia Y, Lin Z, He Z, Li C, Zhang Y, Wang J . Effect of Air Pollution on Heart Failure: Systematic Review and Meta-Analysis. Environ Health Perspect. 2023; 131(7):76001. PMC: 10317211. DOI: 10.1289/EHP11506. View

12.

Sharma V, Filip J, Zboril R, Varma R . Natural inorganic nanoparticles--formation, fate, and toxicity in the environment. Chem Soc Rev. 2015; 44(23):8410-23. DOI: 10.1039/c5cs00236b. View

13.

Karpinich N, Caron K . Schlemm's canal: more than meets the eye, lymphatics in disguise. J Clin Invest. 2014; 124(9):3701-3. PMC: 4151199. DOI: 10.1172/JCI77507. View

14.

Calderon-Garciduenas L, Gonzalez-Maciel A, Reynoso-Robles R, Hammond J, Kulesza R, Lachmann I . Quadruple abnormal protein aggregates in brainstem pathology and exogenous metal-rich magnetic nanoparticles (and engineered Ti-rich nanorods). The substantia nigrae is a very early target in young urbanites and the gastrointestinal tract a key.... Environ Res. 2020; 191:110139. DOI: 10.1016/j.envres.2020.110139. View

15.

Lin C, Chiu C, Lee P, Chen K, He C, Hsu S . The Adverse Effects of Air Pollution on the Eye: A Review. Int J Environ Res Public Health. 2022; 19(3). PMC: 8834466. DOI: 10.3390/ijerph19031186. View

16.

Ahmad E, Lim S, Lamptey R, Webb D, Davies M . Type 2 diabetes. Lancet. 2022; 400(10365):1803-1820. DOI: 10.1016/S0140-6736(22)01655-5. View

17.

Lu D, Luo Q, Chen R, Zhuansun Y, Jiang J, Wang W . Chemical multi-fingerprinting of exogenous ultrafine particles in human serum and pleural effusion. Nat Commun. 2020; 11(1):2567. PMC: 7244483. DOI: 10.1038/s41467-020-16427-x. View

18.

Quintana C, Cowley J, Marhic C . Electron nanodiffraction and high-resolution electron microscopy studies of the structure and composition of physiological and pathological ferritin. J Struct Biol. 2004; 147(2):166-78. DOI: 10.1016/j.jsb.2004.03.001. View

19.

Antonetti D, Silva P, Stitt A . Current understanding of the molecular and cellular pathology of diabetic retinopathy. Nat Rev Endocrinol. 2021; 17(4):195-206. PMC: 9053333. DOI: 10.1038/s41574-020-00451-4. View

20.

Muruganandam N, Mahalingam S, Narayanan R, Rajadurai E . Meandered and muddled: a systematic review on the impact of air pollution on ocular health. Environ Sci Pollut Res Int. 2023; 30(24):64872-64890. DOI: 10.1007/s11356-023-27079-x. View