Effects of particulate matter exposure on the expression of the SARS-CoV-2 ACE2 receptor in ocular surface tissues and cells.
ACE2
CD147
Ocular surface
Particulate matter
SARS-CoV-2
Journal
Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769
Informations de publication
Date de publication:
05 Jan 2024
05 Jan 2024
Historique:
received:
04
10
2023
accepted:
14
12
2023
medline:
5
1
2024
pubmed:
5
1
2024
entrez:
5
1
2024
Statut:
aheadofprint
Résumé
Particulate matter (PM) has been reported to be one of the risk factor for COVID-19 caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). However, although the ocular surface is deeply affected by both PM exposure and SARS-COV-2 infection, no studies have investigated the effects of PM exposure on the ocular route of SARS-COV-2 infection. To this end, we explored the effects of PM on the expression of SARS-COV-2-associated receptors and proteins in ocular surface. Herein, short- and long-term PM-exposed rat models were established by topically administering PM for 3 and 10 days, respectively. Immortalized human corneal epithelial cells (HCECs) and human conjunctival epithelial cells (HCjECs) were exposed to PM. ACE2, TMPRSS2, CD147, and ADAM17 expression levels were measured by western blot analysis. Our results show that short-term PM exposure had little effect on the expressions of ACE2, TMPRSS2, and CD147 in ocular surface tissues. However, long-term PM exposure decreased the ACE2 expression in conjunctival tissues and increased the CD147 expression in corneal or conjunctival tissues. PM exposure reduced the ACE2 expression by increasing the ADAM17 expression and ACE2 shedding level in HCECs and HCjECs. Our findings suggest that long-term PM exposure down-regulate the expression of the SARS-CoV-2 receptor ACE2 in conjunctival tissues through ADAM17-dependent ACE2 shedding. However, long-term PM exposure up-regulates the expression of another SARS-CoV-2 receptor CD147 in ocular surface tissues, accompanied by ocular surface damage and cytotoxicity. This study provides a new insight into uncovering potential risk factors for infection with SARS-CoV-2 via the ocular route.
Identifiants
pubmed: 38180673
doi: 10.1007/s11356-023-31607-0
pii: 10.1007/s11356-023-31607-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Korean Ministry of Environment
ID : 2022003310001
Organisme : National Research Foundation of Korea
ID : NRF-2021R1F1A1047497
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Ali N, Islam F (2020) The Effects of Air Pollution on COVID-19 Infection and Mortality-A Review on Recent Evidence. Front Public Health 8:580057
Alves M, Asbell P, Dogru M, Giannaccare G, Grau A, Gregory D, Kim DH, Marini MC, Ngo W, Nowinska A, Saldanha IJ, Villani E, Wakamatsu TH, Yu M, Stapleton F (2023) TFOS Lifestyle Report: Impact of environmental conditions on the ocular surface. Ocul Surf 29:1–52
Biswas C, Zhang Y, DeCastro R, Guo H, Nakamura T, Kataoka H, Nabeshima K (1995) The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res 55:434–439
Cantero-Navarro E, Fernandez-Fernandez B, Ramos AM, Rayego-Mateos S, Rodrigues-Diez RR, Sanchez-Nino MD, Sanz AB, Ruiz-Ortega M, Ortiz A (2021) Renin-angiotensin system and inflammation update. Mol Cell Endocrinol 529:111254
Chen Q, Li Y, Bie B, Zhao B, Zhang Y, Fang S, Li S, Zhang Y (2023) P38 MAPK activated ADAM17 mediates ACE2 shedding and promotes cardiac remodeling and heart failure after myocardial infarction. Cell Commun Signal 21:73
Chhabra KH, Pedersen KB, Xia H, Shenoy V, Raizada MK, Lazartigues E (2013) Pancreatic ACE2 shedding is associated with impaired glycemia in high fat diet‐fed mice. Wiley Online Library
Chodavarapu H, Pedersen K, Lazartigues E (2015) The ACE2 Sheddase, ADAM17, is Up-Regulated in Diabetic db/db Mice. FASEB J 29(997):1
Dang Z, Su S, Jin G, Nan X, Ma L, Li Z, Lu D, Ge R (2020) Tsantan Sumtang attenuated chronic hypoxia-induced right ventricular structure remodeling and fibrosis by equilibrating local ACE-AngII-AT1R/ACE2-Ang1-7-Mas axis in rat. J Ethnopharmacol 250:112470
D'Ardes D, Boccatonda A, Rossi I, Guagnano MT, Santilli F, Cipollone F, Bucci M (2020) COVID-19 and RAS: Unravelling an Unclear Relationship. Int J Mol Sci 21
de Freitas Santoro D, de Sousa LB, Camara NOS, de Freitas D, de Oliveira LA (2021) SARS-COV-2 and Ocular Surface: From Physiology to Pathology, a Route to Understand Transmission and Disease. Front Physiol 12:612319
Domingo JL, Marques M, Rovira J (2020) Influence of airborne transmission of SARS-CoV-2 on COVID-19 pandemic. A Review. Environ Res 188:109861
Du X, Zeng X, Zhang J, Pan K, Song L, Zhou J, Zhou L, Xie Y, Sun Q, Ge W, Chen R, Zhao J, Kan H (2020) Ambient fine particulate matter induced the elevation of blood pressure through ACE2/Ang(1–7) pathway: The evidence from urine metabolites. Ecotoxicol Environ Saf 203:111044
Ehre C, Worthington EN, Liesman RM, Grubb BR, Barbier D, O’Neal WK, Sallenave JM, Pickles RJ, Boucher RC (2012) Overexpressing mouse model demonstrates the protective role of Muc5ac in the lungs. Proc Natl Acad Sci U S A 109:16528–16533
Endo Y, Hickerson BT, Ilyushina NA, Mohan N, Peng H, Takeda K, Donnelly RP, Wu WJ (2022) Identification of a pharmacological approach to reduce ACE2 expression and development of an in vitro COVID-19 viral entry model. J Virus Erad 8:100307
Feng P, Wu Z, Liu H, Shen Y, Yao X, Li X, Shen Z (2020) Electroacupuncture Improved Chronic Cerebral Hypoperfusion-Induced Anxiety-Like Behavior and Memory Impairments in Spontaneously Hypertensive Rats by Downregulating the ACE/Ang II/AT1R Axis and Upregulating the ACE2/Ang-(1–7)/MasR Axis. Neural Plast 2020:9076042
Gabison EE, Mourah S, Steinfels E, Yan L, Hoang-Xuan T, Watsky MA, De Wever B, Calvo F, Mauviel A, Menashi S (2005) Differential expression of extracellular matrix metalloproteinase inducer (CD147) in normal and ulcerated corneas: role in epithelio-stromal interactions and matrix metalloproteinase induction. Am J Pathol 166:209–219
Gabison EE, Huet E, Baudouin C, Menashi S (2009) Direct epithelial-stromal interaction in corneal wound healing: Role of EMMPRIN/CD147 in MMPs induction and beyond. Prog Retin Eye Res 28:19–33
Gallagher TM, Buchmeier MJ (2001) Coronavirus spike proteins in viral entry and pathogenesis. Virology 279:371–374
Haga S, Yamamoto N, Nakai-Murakami C, Osawa Y, Tokunaga K, Sata T, Yamamoto N, Sasazuki T, Ishizaka Y (2008) Modulation of TNF-alpha-converting enzyme by the spike protein of SARS-CoV and ACE2 induces TNF-alpha production and facilitates viral entry. Proc Natl Acad Sci U S A 105:7809–7814
Hoffmann M, Kleine-Weber H, Schroeder S, Kruger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu NH, Nitsche A, Muller MA, Drosten C, Pohlmann S (2020) SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell 181(271–280):e8
Hussain M, Jabeen N, Amanullah A, Baig AA, Aziz B, Shabbir S, Raza F, Uddin N (2020) Molecular docking between human TMPRSS2 and SARS-CoV-2 spike protein: conformation and intermolecular interactions. AIMS Microbiol 6:350–360
Hyun SW, Song SJ, Park B, Lee TG, Kim CS (2020) Toxicological effects of urban particulate matter on corneal and conjunctival epithelial cells. Toxicol Res 36:311–318
Hyun SW, Kim J, Park B, Jo K, Lee TG, Kim JS, Kim CS (2019) Apricot Kernel Extract and Amygdalin Inhibit Urban Particulate Matter-Induced Keratoconjunctivitis Sicca. Molecules 24
Jackson CB, Farzan M, Chen B, Choe H (2022) Mechanisms of SARS-CoV-2 entry into cells. Nat Rev Mol Cell Biol 23:3–20
Jiang Z, Zhang H, Gao J, Yu H, Han R, Zhu L, Chen X, Fan Q, Hao P, Wang L, Li X (2021) ACE2 Expression Is Upregulated in Inflammatory Corneal Epithelial Cells and Attenuated by Resveratrol. Invest Ophthalmol vis Sci 62:25
Lambert DW, Yarski M, Warner FJ, Thornhill P, Parkin ET, Smith AI, Hooper NM, Turner AJ (2005) Tumor necrosis factor-alpha convertase (ADAM17) mediates regulated ectodomain shedding of the severe-acute respiratory syndrome-coronavirus (SARS-CoV) receptor, angiotensin-converting enzyme-2 (ACE2). J Biol Chem 280:30113–30119
Lan J, Ge J, Yu J, Shan S, Zhou H, Fan S, Zhang Q, Shi X, Wang Q, Zhang L, Wang X (2020) Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor. Nature 581:215–220
Lavrentyev EN, Malik KU (2009) High glucose-induced Nox1-derived superoxides downregulate PKC-betaII, which subsequently decreases ACE2 expression and ANG(1–7) formation in rat VSMCs. Am J Physiol Heart Circ Physiol 296:H106–H118
Lee TG, Hyun SW, Jo K, Park B, Lee IS, Song SJ, Kim CS (2019) Achyranthis radix Extract Improves Urban Particulate Matter-Induced Dry Eye Disease. Int J Environ Res Public Health 16
Leonardi A, Rosani U, Brun P (2020) Ocular Surface Expression of SARS-CoV-2 Receptors. Ocul Immunol Inflamm 28:735–738
Li X, Kang B, Woo IH, Eom Y, Lee HK, Kim HM, Song JS (2018) Effects of Topical Mucolytic Agents on the Tears and Ocular Surface: A Plausible Animal Model of Mucin-Deficient Dry Eye. Invest Ophthalmol vis Sci 59:3104–3114
Li X, Kang B, Eom Y, Lee HK, Kim HM, Song JS (2020) The Protective Effect of an Eye Wash Solution on the Ocular Surface Damage Induced by Airborne Carbon Black Exposure. Cornea 39:1040–1047
Li HH, Liu CC, Hsu TW, Lin JH, Hsu JW, Li AF, Yeh YC, Hung SC, Hsu HS (2021) Upregulation of ACE2 and TMPRSS2 by particulate matter and idiopathic pulmonary fibrosis: a potential role in severe COVID-19. Part Fibre Toxicol 18:11
Li X, Kang B, Eom Y, Zhong J, Lee HK, Kim HM, Song JS (2022a) SIRT1 Protects Against Particulate Matter-Induced Oxidative Stress in Human Corneal and Conjunctival Epithelial Cells. Invest Ophthalmol vis Sci 63:19
Li X, Kang B, Eom Y, Zhong J, Lee HK, Kim HM, Song JS (2022b) Comparison of cytotoxicity effects induced by four different types of nanoparticles in human corneal and conjunctival epithelial cells. Sci Rep 12:155
Lu C-W, Liu X-F, Jia Z-F (2020) 2019-nCoV transmission through the ocular surface must not be ignored. Lancet (london, England) 395:e39
Ma D, Chen CB, Jhanji V, Xu C, Yuan XL, Liang JJ, Huang Y, Cen LP, Ng TK (2020) Expression of SARS-CoV-2 receptor ACE2 and TMPRSS2 in human primary conjunctival and pterygium cell lines and in mouse cornea. Eye (lond) 34:1212–1219
Martinez-Carrasco R, Argueso P, Fini ME (2021) Membrane-associated mucins of the human ocular surface in health and disease. Ocul Surf 21:313–330
McAuley JL, Corcilius L, Tan HX, Payne RJ, McGuckin MA, Brown LE (2017) The cell surface mucin MUC1 limits the severity of influenza A virus infection. Mucosal Immunol 10:1581–1593
Moreira de Queiroz T, Sriramula S, Chaudhari A, Filipeanu C, Lazartigues E (2014) Angiotensin-II promotes ACE2 shedding by increasing ADAM17 expression and oxidative stress in Neuro2A cells (874.10). FASEB J 28(874):10
Niu L, Li L, Xing C, Luo B, Hu C, Song M, Niu J, Ruan Y, Sun X, Lei Y (2021) Airborne particulate matter (PM(2.5)) triggers cornea inflammation and pyroptosis via NLRP3 activation. Ecotoxicol Environ Saf 207:111306
Patel VB, Clarke N, Wang Z, Fan D, Parajuli N, Basu R, Putko B, Kassiri Z, Turner AJ, Oudit GY (2014) Angiotensin II induced proteolytic cleavage of myocardial ACE2 is mediated by TACE/ADAM-17: a positive feedback mechanism in the RAS. J Mol Cell Cardiol 66:167–176
Qiao J, Li W, Bao J, Peng Q, Wen D, Wang J, Sun B (2020) The expression of SARS-CoV-2 receptor ACE2 and CD147, and protease TMPRSS2 in human and mouse brain cells and mouse brain tissues. Biochem Biophys Res Commun 533:867–871
Qu JY, Xie HT, Zhang MC (2021) Evidence of SARS-CoV-2 Transmission Through the Ocular Route. Clin Ophthalmol 15:687–696
Sagawa T, Tsujikawa T, Honda A, Miyasaka N, Tanaka M, Kida T, Hasegawa K, Okuda T, Kawahito Y, Takano H (2021) Exposure to particulate matter upregulates ACE2 and TMPRSS2 expression in the murine lung. Environ Res 195:110722
Saheb Sharif-Askari N, Saheb Sharif-Askari F, Alabed M, Temsah MH, Al Heialy S, Hamid Q, Halwani R (2020) Airways Expression of SARS-CoV-2 Receptor, ACE2, and TMPRSS2 Is Lower in Children Than Adults and Increases with Smoking and COPD. Mol Ther Methods Clin Dev 18:1–6
Santos RX, Correia SC, Alves MG, Oliveira PF, Cardoso S, Carvalho C, Duarte AI, Santos MS, Moreira PI (2014) Insulin therapy modulates mitochondrial dynamics and biogenesis, autophagy and tau protein phosphorylation in the brain of type 1 diabetic rats. Biochim Biophys Acta 1842:1154–1166
Scialo F, Daniele A, Amato F, Pastore L, Matera MG, Cazzola M, Castaldo G, Bianco A (2020) ACE2: The Major Cell Entry Receptor for SARS-CoV-2. Lung 198:867–877
Shilts J, Crozier TWM, Greenwood EJD, Lehner PJ, Wright GJ (2021) No evidence for basigin/CD147 as a direct SARS-CoV-2 spike binding receptor. Sci Rep 11:413
Shimmura S, Ono M, Shinozaki K, Toda I, Takamura E, Mashima Y, Tsubota K (1995) Sodium hyaluronate eyedrops in the treatment of dry eyes. Br J Ophthalmol 79:1007–1011
Somayajulu M, McClellan SA, Wright R, Pitchaikannu A, Croniger B, Zhang K, Hazlett LD (2023) Airborne Exposure of the Cornea to PM(10) Induces Oxidative Stress and Disrupts Nrf2 Mediated Anti-Oxidant Defenses. Int J Mol Sci 24
Song SJ, Hyun SW, Lee TG, Park B, Jo K, Lee IS, Kim CS (2019) Topical Application of Liriope platyphylla Extract Attenuates Dry Eye Syndrome Induced by Particulate Matter. J Ophthalmol 2019:1429548
Thunders M, Delahunt B (2020) Gene of the month: TMPRSS2 (transmembrane serine protease 2). J Clin Pathol 73:773–776
Wakabayashi H, Oda H, Yamauchi K, Abe F (2014) Lactoferrin for prevention of common viral infections. J Infect Chemother 20:666–671
Wang X, Wang CP, Hu QH, Lv YZ, Zhang X, Ouyang Z, Kong LD (2010) The dual actions of Sanmiao wan as a hypouricemic agent: down-regulation of hepatic XOD and renal mURAT1 in hyperuricemic mice. J Ethnopharmacol 128:107–115
Wang J, Kaplan N, Wysocki J, Yang W, Lu K, Peng H, Batlle D, Lavker RM (2020a) The ACE2-deficient mouse: A model for a cytokine storm-driven inflammation. FASEB J 34:10505–10515
Wang K et al (2020b) CD147-spike protein is a novel route for SARS-CoV-2 infection to host cells. Signal Transduct Target Ther 5:283
Wise S, Watters RJGMD (2008) Standard Reference Material 1648a, certificate of analysis
Wu X, Nethery RC, Sabath BM, Braun D, Dominici F (2020) Exposure to air pollution and COVID-19 mortality in the United States: A nationwide cross-sectional study. medRxiv
Xiao F, Zimpelmann J, Agaybi S, Gurley SB, Puente L, Burns KD (2014) Characterization of angiotensin-converting enzyme 2 ectodomain shedding from mouse proximal tubular cells. PLoS One 9:e85958
Xiao F, Zimpelmann J, Burger D, Kennedy C, Hebert RL, Burns KD (2016) Protein Kinase C-delta Mediates Shedding of Angiotensin-Converting Enzyme 2 from Proximal Tubular Cells. Front Pharmacol 7:146
Xu J, Sriramula S, Lazartigues E (2018) Excessive Glutamate Stimulation Impairs ACE2 Activity Through ADAM17-Mediated Shedding in Cultured Cortical Neurons. Cell Mol Neurobiol 38:1235–1243
Yan R, Zhang Y, Li Y, Xia L, Guo Y, Zhou Q (2020) Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science 367:1444–1448
Yoon S, Han S, Jeon KJ, Kwon S (2018) Effects of collected road dusts on cell viability, inflammatory response, and oxidative stress in cultured human corneal epithelial cells. Toxicol Lett 284:152–160
Zhang H, Penninger JM, Li Y, Zhong N, Slutsky AS (2020) Angiotensin-converting enzyme 2 (ACE2) as a SARS-CoV-2 receptor: molecular mechanisms and potential therapeutic target. Intensive Care Med 46:586–590
Zhou L, Xu Z, Castiglione GM, Soiberman US, Eberhart CG, Duh EJ (2020) ACE2 and TMPRSS2 are expressed on the human ocular surface, suggesting susceptibility to SARS-CoV-2 infection. Ocul Surf 18:537–544
Zhu TY, Qiu H, Cao QQ, Duan ZL, Liu FL, Song TZ, Liu Y, Fang YQ, Wu GM, Zheng YT, Ding WJ, Lai R, Jin L (2021) Particulate matter exposure exacerbates susceptibility to SARS-CoV-2 infection in humanized ACE2 mice. Zool Res 42:335–338