All Issue

2022 Vol.52, Issue 3

Review Article

Impact of Ambient Particulate Matter on the Skin’s Immune System
Abdur Rehman1
,
Young-Sang Koh1*
1Department of Microbiology and Immunology, College of Medicine, and Jeju Research Center for Natural Medicine, Jeju National University, Jeju 63243, Republic of Korea
*yskoh7@jejunu.ac.kr
30 September 2022. pp. 83-93
PDF XML Citation
Abstract

Skin is the outermost layer of the human body. The main functions of the skin include protecting the body from external harm, maintaining homeostasis, sensory perception, and thermoregulation. The skin contains many immune cells that participate both in innate and adaptive immunity. Proper skin function is disrupted when exposed to harmful environmental pollutants, such as airborne particulate matter, which aggravates the severity of skin diseases, such as eczema, psoriasis, and atopic dermatitis. Air pollution kills approximately five million individuals annually, and the death rate continues to rise. Many studies have been conducted regarding the role of particulate matter in the respiratory system. In contrast, there is minimal data available on the impact of particulate matter on the skin’s immune system. However, there is more information available in recent years; for instance, PM exposure impairs skin barrier function by activating different inflammatory pathways, dysregulates T cell differentiation, activates NLRP3 inflammasome, and induces pro-inflammatory cytokine secretion. Therefore, this review assiduously discusses the impact of ambient particulate matter on the skin’s immune system.

Keywords
Particulate matter
Skin immune system
Toll-like receptor
Inflammasome
References
1

Kanitakis J. Anatomy, histology and immunohistochemistry of normal human skin. Eur J Dermatol 2002;12:390-9.

2

Murphy GF. Histology of the Skin. In: Elenitsas R, Jaworsky C, Johnson B, editors. Lever's Histopathology of the Skin. 11th ed. Philadelphia:Lippincott-Raven;1997. p.5-45.

3

Nguyen AV, Soulika AM. The Dynamics of the Skin's Immune System. Int J Mol Sci 2019;20:1811.

10.3390/ijms2008181131013709PMC6515324
4

Kawai T, Akira S. Pathogen recognition with Toll-like receptors. Curr Opin Immunol 2005;17:338-44.

10.1016/j.coi.2005.02.00715950447
5

Zhong Y, Kinio A, Saleh M. Functions of NOD-Like receptors in human diseases. Front Immunol 2013;4:333.

10.3389/fimmu.2013.0033324137163PMC3797414
6

Tang D, Kang R, Coyne CB, Zeh HJ, Lotze MT. PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol Rev 2012;249:158-75.

10.1111/j.1600-065X.2012.01146.x22889221PMC3662247
7

Franchi L, Park JH, Shaw MH, Marina-Garcia N, Chen G, Kim YG, et al. Intracellular NOD-like receptors in innate immunity, infection and disease. Cell Microbiol 2008;10:1-8.

8

Adams K, Greenbaum DS, Shaikh R, Erp AM, Russell AG. Particulate matter components, sources, and health: systematic approaches to testing effects. J Air Waste Manag Assoc 2015;65:544-58.

10.1080/10962247.2014.100188425947313
9

Jung S, Lim J, Kwon S, Jeon S, Kim J, Lee J, et al. Characterization of particulate matter from diesel passenger cars tested on chassis dynamometers. J Environ Sci 2017;54:21-32.

10.1016/j.jes.2016.01.03528391931
10

Ain NU, Qamar SUR. Particulate matter-induced cardiovascular dysfunction: a mechanistic insight. Cardiovasc Toxicol 2021;21:505-16.

10.1007/s12012-021-09652-333886046
11

Sompornrattanaphan M, Thongngarm T, Ratanawatkul P, Wongsa C, Swigris JJ. The contribution of particulate matter to respiratory allergy. Asian Pac J Allergy Immunol 2020;38:19-28.

12

Berardesca E, Farage M, Maibach H. Sensitive skin: an overview. Int J Cosmet Sci 2013;35:2-8

10.1111/j.1468-2494.2012.00754.x22928591
13

Tsuji G, Takahara M, Uchi H, Takeuchi S, Mitoma C, Moroi Y, et al. An environ mental contaminant, benzo(a)pyrene, induces oxidative stress-mediated interleukin-8 production in human keratinocytes via the aryl hydrocarbon receptor signalling pathway. J Dermatol Sci 2011;62:42-9.

10.1016/j.jdermsci.2010.10.017
14

Jeong SH, Park JH, Kim JN, Park YH, Shin SY, Lee YH, et al. Up-regulation of TNF-alpha secretion by cigarette smoke is mediated by Egr-1 in HaCaT human keratinocytes. Exp Dermatol 2010;19:206-12.

10.1111/j.1600-0625.2009.01050.x20653771
15

Arkwright PD, Motala C, Subramanian H, Spergel J, Schneider LC, Wollenberg A, et al. Management of difficult-to- treat atopic dermatitis. J Allergy Clin Immunol Pract 2013;1:142-51.

10.1016/j.jaip.2012.09.00224565453
16

Wolter S, Price HN. Atopic dermatitis. Pediatr Clin North Am 2014;61:241-60.

10.1016/j.pcl.2013.11.00224636644
17

Kimata H. Exposure to road traffic enhances allergic skin wheal responses and increases plasma neuropeptides and neurotrophins in patients with atopic eczema/dermatitis syndrome. Int J Hyg Environ Health 2004;207:45-9.

10.1078/1438-4639-0026114762973
18

Schmitz R, Atzpodien K, Schlaud M. Prevalence and risk factors of atopic diseases in German children and adolescents. Pediatr Allergy Immunol 2012;23:716-23.

10.1111/j.1399-3038.2012.01342.x22882467
19

Flohr C, Mann J. New approaches to the prevention of childhood atopic dermatitis. Allergy 2014;69:56-61.

10.1111/all.1234324372089
20

Thomsen SF, Ulrik CS, Kyvik KO, Hjelmborg J, Skadhauge LR, Steffensen I, et al. Importance of genetic factors in the etiology of atopic dermatitis: a twin study. Allergy Asthma Proc 2007;28:535-9.

10.2500/aap2007.28.304118034971
21

Morgenstern V, Zutavern A, Cyrys J, Brockow I, Koletzko S, Krämer U, et al. Atopic diseases, allergic sensitization, and exposure to traffic-related air pollution in children. Am J Respir Crit Care Med 2008;177:1331-7.

10.1164/rccm.200701-036OC18337595
22

Guarnieri M, Balmes JR. Outdoor air pollution and asthma. Lancet 2014;383:1581-92.

10.1016/S0140-6736(14)60617-6
23

Kim KE, Cho D, Park HJ. Air pollution and skin diseases: adverse effects of airborne particulate matter on various skin diseases. Life Sci 2016;152:126-34.

10.1016/j.lfs.2016.03.03927018067
24

Dijkhoff IM, Drasler B, Karakocak BB, Petri-Fink A, Valacchi G, Eeman M, et al. Impact of airborne particulate matter on skin: a systematic review from epidemiology to in vitro studies. Part Fibre Toxicol 2020;17:35.

10.1186/s12989-020-00366-y32711561PMC7382801
25

Swann G. The skin is the body's largest organ. J Vis Commun Med 2010;33:148-9.

26

Proksch E, Brandner JM, Jensen JM. The skin: an indispensable barrier. Exp Dermatol 2008;17:1063-72.

10.1111/j.1600-0625.2008.00786.x19043850
27

Stücker M, Struk A, Altmeyer P, Herde M, Baumgärtl H, Lübbers DW. The cutaneous uptake of atmospheric oxygen contributes significantly to the oxygen supply of human dermis and epidermis. J Physiol 2002;538:985-94.

10.1113/jphysiol.2001.01306711826181PMC2290093
28

Haftek M. The stratum corneum. Ann Dermatol Venereol 2002;129:117-22.

29

Wong R, Geyer S, Weninger W, Guimberteau JC, Wong JK. The dynamic anatomy and patterning of skin. Exp Dermatol 2016;25:92-8.

10.1111/exd.1283226284579
30

Jensen JM, Proksch E. The skin's barrier. G Ital Dermatol Venereol 2009;144:689-700.

31

Oh J, Byrd AL, Deming C, Conlan S, Kong HH, Segre JA. Biogeography and individuality shape function in the human skin metagenome. Nature 2014;514:59-64.

10.1038/nature1378625279917PMC4185404
32

Zook EC, Kee BL. Development of innate lymphoid cells. Nat Immunol 2016;17:775-82.

10.1038/ni.348127328007
33

Matejuk A. Skin immunity. Arch Immunol Ther Exp 2018;66:45-54.

10.1007/s00005-017-0477-328623375PMC5767194
34

Leonard WJ. TSLP: finally in the limelight. Nat Immunol 2002;3:605-7.

10.1038/ni0702-60512087416
35

Ho AW, Kupper TS. T cells and the skin: from protective immunity to inflammatory skin disorders. Nat Rev Immunol 2019;19:490-502.

10.1038/s41577-019-0162-330992525
36

Nestle FO, Meglio PD, Qin JZ, Nickoloff BJ. Skin immune sentinels in health and disease. Nat Rev Immunol 2009;9:679-91.

10.1038/nri262219763149PMC2947825
37

Cua DJ, Tato CM. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 2010;10:479-89.

10.1038/nri280020559326
38

Nickel J, Dijke PT, Mueller TD. TGF-β family co-receptor function and signaling. Acta Biochim Biophys Sin 2018;50:12-36.

10.1093/abbs/gmx12629293886
39

Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nat Rev Microbiol 2018;16:143-55.

10.1038/nrmicro.2017.15729332945
40

Bates JT, Fang T, Verma V, Zeng L, Weber RJ , Tolbert PE, et al. Review of acellular assays of ambient particulate matter oxidative potential: methods and relationships with composition, sources, and health effects. Environ Sci Technol 2019;53:4003-19.

10.1021/acs.est.8b0343030830764
41

Srimuruganandam B, Shiva Nagendra SM. Source characterization of PM10 and PM2.5 mass using a chemical mass balance model at urban roadside. Sci Total Environ 2012;433:8-19.

10.1016/j.scitotenv.2012.05.08222766423
42

Sarigiannis DΑ, Karakitsios SP, Kermenidou M, Nikolaki S, Zikopoulos D, Semelidis S, et al. Total exposure to airborne particulate matter in cities: the effect of biomass combustion. Sci Total Environ 2014;493:795-805

10.1016/j.scitotenv.2014.06.05525000575
43

Fuller R, Landrigan PJ, Balakrishnan K, Bathan G, Bose-O'Reilly S, Brauer M, et al. Pollution and health: a progress update. Lancet Planet Health 2022;6:e535-47.

10.1016/S2542-5196(22)00090-0
44

Mukherjee A, Agrawal M. A global perspective of fine particulate matter Pollution and its health effects. Rev Environ Contam Toxicol 2018;244:5-51.

10.1007/398_2017_328361472
45

Du Y, Xu X, Chu M, Guo Y, Wang J. Air particulate matter and cardiovascular disease: the epidemiological, biomedical and clinical evidence. J Thorac Dis 2016;8:E8-19.

46

Krutmann J, Liu W, Li L, Pan X, Crawford M, Sore G, et al. Pollution and skin: From epidemiological and mechanistic studies to clinical implications. J Dermatol Sci 2014;76:163-8.

10.1016/j.jdermsci.2014.08.00825278222
47

Ravindra K, Sokhi R, Grieken RV. Atmospheric polycyclic aromatic hydrocarbons: Source attribution, emission factors and regulation. Atmos Environ 2008;42:2895-921.

10.1016/j.atmosenv.2007.12.010
48

Tang NJ, Liu J, Coenraads PJ, Dong L, Zhao LJ, Ma SW, et al. Expression of AhR, CYP1A1, GSTA1, c-fos and TGF-alpha in skin lesions from dioxin-exposed humans with chloracne. Toxicol Lett 2008;177:182-7.

10.1016/j.toxlet.2008.01.01118329192
49

Magnani ND, Muresan XM, Belmonte G, Cervellati F, Sticozzi C, Pecorelli A, et al. Skin damage mechanisms related to airborne particulate matter exposure. Toxicol Sci 2016;149:227-36.

10.1093/toxsci/kfv23026507108
50

Costa C, Catania S, De Pasquale R, Stancanelli R, Scribano GM, Melchini A. Exposure of human skin to benzo [a]pyrene: Role of CYP1A1 and aryl hydrocarbon receptor in oxidative stress generation. Toxicology 2010;271:83-6.

10.1016/j.tox.2010.02.01420307623
51

Johnson NM, Hoffmann AR, Behlen JC, Lau C, Pendleton D, Harvey N, et al. Air pollution and children's health-a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter. Environ Health Prev Med 2021;26:72.

10.1186/s12199-021-00995-534253165PMC8274666
52

Yang SI. Particulate matter and childhood allergic diseases. Korean J Pediatr 2019;62:22-29.

10.3345/kjp.2018.0704530404430PMC6351801
53

Guaita R, Pichiule M, Maté T, Linares C, Díaz J. Short-term impact of particulate matter (PM(2.5)) on respiratory mortality in Madrid. Int J Environ Health Res 2011;21:260-74.

10.1080/09603123.2010.54403321644129
54

Peng W, Novak N. Pathogenesis of atopic dermatitis. Clin Exp Allergy 2015;45:566-74.

10.1111/cea.1249525610977
55

Weidinger S, Novak N. Atopic dermatitis. Lancet 2016;387:1109-22.

10.1016/S0140-6736(15)00149-X
56

Cork MJ, Danby SG, Vasilopoulos Y, Hadgraft J, Lane ME, Moustafa M, et al. Epidermal barrier dysfunction in atopic dermatitis. J Invest Dermatol 2009;129:1892-908.

10.1038/jid.2009.13319494826
57

Kim BE, Leung DY, Boguniewicz M, Howell MD. Loricrin and involucrin expression is down-regulated by Th2 cytokines through STAT-6. Clin Immunol 2008;126:332-7.

10.1016/j.clim.2007.11.00618166499PMC2275206
58

Kim K, Kim H, Sung GY. An interleukin-4 and interleukin-13 induced atopic dermatitis human skin equivalent model by a skin-on-a-chip. Int J Mol Sci 2022;23:2116.

10.3390/ijms2304211635216228PMC8878506
59

Kamsteeg M, Bergers M, de Boer R, Zeeuwen PL, Hato SV, Schalkwijk J, et al. Type 2 helper T-cell cytokines induce morphologic and molecular characteristics of atopic dermatitis in human skin equivalent. Am J Pathol 2011;178:2091-9.

10.1016/j.ajpath.2011.01.03721514424PMC3081201
60

Song S, Lee K, Lee YM, Lee JH, Lee SI, Yu SD, et al. Acute health effects of urban fine and ultrafine particles on children with atopic dermatitis. Environ Res 2011;111:394-9.

10.1016/j.envres.2010.10.01021367405
61

Ahn K. The role of air pollutants in atopic dermatitis. J Allergy Clin Immunol 2014;134:993-9

10.1016/j.jaci.2014.09.02325439225
62

Hassoun Y, James C, Bernstein DI. The effects of air pollution on the development of atopic disease. Clin Rev Allergy Immunol 2019;57:403-14.

10.1007/s12016-019-08730-330806950PMC8215519
63

Kim J, Kim EH, Oh I, Jung K, Han Y, Cheong HK, et al. Symptoms of atopic dermatitis are influenced by outdoor air pollution. J Allergy Clin Immunol 2013;132:495-8.

10.1016/j.jaci.2013.04.01923763977
64

Leung DY, Berdyshev E, Goleva E. Cutaneous barrier dysfunction in allergic diseases. J Allergy Clin Immunol 2020;145:1485-97.

10.1016/j.jaci.2020.02.02132507227PMC7291847
65

Ho PP, Steinman L. The aryl hydrocarbon receptor: a regulator of Th17 and Treg cell development in disease. Cell Res 2008;18:605-8.

10.1038/cr.2008.6318516065
66

Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235-8.

10.1038/nature0475316648838
67

Quintana FJ, Basso AS, Iglesias AH, Korn T, Farez MF, Bettelli E, et al. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 2008;453:65-71.

10.1038/nature0688018362915
68

Gutiérrez-Vázquez C, Quintana FJ. Regulation of the Immune Response by the Aryl Hydrocarbon Receptor. Immunity 2018;48:19-33.

10.1016/j.immuni.2017.12.01229343438PMC5777317
69

Ehrlich AK, Pennington JM, Bisson WH, Kolluri SK, Kerkvliet NI. TCDD, FICZ, and other high affinity AhR ligands dose-dependently determine the fate of CD4+ T cell differentiation. Toxicol Sci 2018;161:310-20.

10.1093/toxsci/kfx21529040756PMC5837604
70

van Voorhis M, Knopp S, Julliard W, Fechner JH, Zhang X, Schauer JJ, et al. Exposure to atmospheric particulate matter enhances Th17 polarization through the aryl hydrocarbon receptor. PLoS One 2013;8:e82545.

10.1371/journal.pone.008254524349309PMC3859609
71

Matthews NC, Pfeffer PE, Mann EH, Kelly FJ, Corrigan CJ, Hawrylowicz CM, et al. Urban particulate matter-activated human dendritic cells induce the expansion of potent inflammatory Th1, Th2, and Th17 effector cells. Am J Respir Cell Mol Biol 2016;54:250-62.

10.1165/rcmb.2015-0084OC26196219PMC4821044
72

Castan͂eda AR, Pinkerton KE, Bein KJ, Magan͂a-Méndez A, Yang HT, Vogel CFA, et al. Ambient particulate matter activates the aryl hydrocarbon receptor in dendritic cells and enhances Th17 polarization. Toxicol Lett 2018;292:85-96.

10.1016/j.toxlet.2018.04.02029689377PMC5971007
73

Matthews NC, Faith A, Pfeffer P, Lu H, Kelly FJ, Hawrylowicz CM, et al. Urban particulate matter suppresses priming of T helper type 1 cells by granulocyte/macrophage colony-stimulating factor-activated human dendritic cells. Am J Respir Cell Mol Biol 2014;50:281-91.

10.1165/rcmb.2012-0465OC24010813
74

O'Driscoll CA, Gallo ME, Hoffmann EJ, Fechner JH, Schauer JJ, Bradfield CA, et al. Polycyclic aromatic hydrocarbons (PAHs) present in ambient urban dust drive proinflammatory T cell and dendritic cell responses via the aryl hydrocarbon receptor (AHR) in vitro. PLoS One 2018;13:e0209690.

10.1371/journal.pone.020969030576387PMC6303068
75

Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 2014;20:1126-67.

10.1089/ars.2012.514923991888PMC3929010
76

Kim M, Kim JH, Jeong GJ, Park KY, Lee MK, Seo SJ. Particulate matter induces pro‐inflammatory cytokines via phosphorylation of p38 MAPK possibly leading to dermal inflammaging. Exp Dermatol 2019;28:809-15.

10.1111/exd.1394331001893
77

Ryu YS, Kang KA, Piao MJ, Ahn MJ, Yi JM, Hyun YM, et al. Particulate matter induces inflammatory cytokine production via activation of NFκB by TLR5-NOX4-ROS signaling in human skin keratinocyte and mouse skin. Redox Biol 2019;21:101080.

10.1016/j.redox.2018.10108030584981PMC6305701
78

Liu T, Zhang L, Joo D, Sun SC. NF-κB signaling in inflammation. Signal Transduct Target Ther 2017;2:17023.

10.1038/sigtrans.2017.2329158945PMC5661633
79

Kitaura J, Asai K, Maeda-Yamamoto M, Kawakami Y, Kikkawa U, Kawakami T. Akt-dependent cytokine production in mast cells. J Exp Med 2000;192:729-40.

10.1084/jem.192.5.72910974038PMC2193272
80

Hers I, Vincent EE, Tavaré JM. Akt signalling in health and disease. Cell Signal 2011;23:1515-27.

10.1016/j.cellsig.2011.05.00421620960
81

Yang Y, Kim SC, Yu T, Yi YS, Rhee MH, Sung GH, et al. Functional roles of p38 mitogen-activated protein kinase in macrophage-mediated inflammatory responses. Mediators Inflamm 2014;2014:352371

10.1155/2014/35237124771982PMC3977509
82

Dhar A, Young MR, Colburn NH. The role of AP-1, NF-kappaB and ROS/NOS in skin carcinogenesis: the JB6 model is predictive. Mol Cell Biochem 2002;234-235:185-93.

10.1007/978-1-4615-1087-1_2112162432
83

Jin SP, Li Z, Choi EK, Lee S, Kim YK, Seo EY, et al. Urban particulate matter in air pollution penetrates into the barrier-disrupted skin and produces ROS-dependent cutaneous inflammatory response in vivo. J Dermatol Sci 2018;S0923-1811:30202-0.

84

Sadakane K, Ichinose T, Takano H, Yanagisawa R, Inoue K, Kawazato H, et al. Organic chemicals in diesel exhaust particles enhance picryl chloride-induced atopic dermatitis in NC/Nga mice. Int Arch Allergy Immunol 2013; 162:7-15.

10.1159/00035076523817207
85

Amores-Iniesta J, Barberà-Cremades M, Martinez CM, Pons JA, Revilla-Nuin B, Martínez-Alarcón L, et al. Extracellular ATP activates the NLRP3 inflammasome and is an early danger signal of skin allograft rejection. Cell Rep 2017;21:3414-26.

10.1016/j.celrep.2017.11.07929262323PMC5746605
86

Sharma J, Parsai K, Raghuwanshi P, Ali SA, Tiwari V, Bhargava A, et al. Emerging role of mitochondria in airborne particulate matter-induced immunotoxicity. Environ Pollut 2021;270:116242.

10.1016/j.envpol.2020.11624233321436
87

Zeng X, Liu D, Wu W, Huo X. PM2.5 exposure inducing ATP alteration links with NLRP3 inflammasome activation. Environ Sci Pollut Res Int 2022;29:24445-56.

10.1007/s11356-021-16405-w35064883PMC8783591
88

Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol 2013;13:397-411.

10.1038/nri345223702978PMC3807999
89

Kim HJ, Bae IH, Son ED, Park J, Cha N, Na HW, et al. Transcriptome analysis of airborne PM2.5-induced detrimental effects on human keratinocytes. Toxicol Lett 2017;273:26-35.

10.1016/j.toxlet.2017.03.01028341207
90

Li Q, Kang Z, Jiang S, Zhao J, Yan S, Xu F, et al. Effects of ambient fine particles PM2.5 on human HaCaT cells. Int J Environ Res Public Health 2017;14:72.

10.3390/ijerph1401007228085100PMC5295323
91

Kim BE, Kim J, Goleva E, Berdyshev E, Lee J, Vang KA, et al. Particulate matter causes skin barrier dysfunction. JCI Insight 2021;6:e145185.

10.1172/jci.insight.14518533497363PMC8021104
Information
  • Publisher :The Korean Society for Microbiology and The Korean Society of Virology
  • Publisher(Ko) :대한미생물학회‧대한바이러스학회
  • Journal Title :JOURNAL OF BACTERIOLOGY AND VIROLOGY
  • Volume : 52
  • No :3
  • Pages :83-93
  • Received Date : 2022-08-29
  • Revised Date : 2022-09-12
  • Accepted Date : 2022-09-19
  • DOI :https://doi.org/10.4167/jbv.2022.52.3.083
Journal Informaiton JOURNAL OF BACTERIOLOGY AND VIROLOGY JOURNAL OF BACTERIOLOGY AND VIROLOGY
  • NRF
  • 임플란트학회 전용 배너
  • KOFST
  • crossref crossmark
  • crossref cited-by
  • crossref funder-registry
  • crosscheck
  • orcid
  • open access
  • ccl
Journal Informaiton Journal Informaiton - close