Changes in Human Peripheral Blood Mononuclear Cell (HPBMC) Populations and T-cell Subsets Associated with Arsenic and Polycyclic Aromatic Hydrocarbon Exposures in a Bangladesh Cohort

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2019 Aug 1

PMID 31365547

Citations 12

Authors

Fredine T Lauer

Faruque Parvez

Pam Factor-Litvak

XinHua Liu

Regina M Santella

Tariqul Islam

Mahbubul Eunus

Nur Alam

A K M Rabiul Hasan

Mizanour Rahman

Habibul Ahsan

Joseph Graziano

Scott W Burchiel

Affiliations

Soon will be listed here.

Abstract

Exposures to environmental arsenic (As) and polycyclic aromatic hydrocarbons (PAH) have been shown to independently cause dysregulation of immune function. Little data exists on the associations between combined exposures to As and PAH with immunotoxicity in humans. In this work we examined associations between As and PAH exposures with lymphoid cell populations in human peripheral blood mononuclear cells (PBMC), as well as alterations in differentiation and activation of B and T cells. Two hundred men, participating in the Health Effects of Arsenic Longitudinal Study (HEALS) in Bangladesh, were selected for the present study based on their exposure to As from drinking water and their cigarette smoking status. Blood and urine samples were collected from study participants. We utilized multiparameter flow cytometry in PBMC to identify immune cells (B, T, monocytes, NK) as well as the T-helper (Th) cell subsets (Th1, Th2, Th17, and Tregs) following ex vivo activation. We did not find evidence of interactions between As and PAH exposures. However, individual exposures (As or PAH) were associated with changes to immune cell populations, including Th cell subsets. Arsenic exposure was associated with an increase in the percentage of Th cells, and dose dependent changes in monocytes, NKT cells and a monocyte subset. Within the Th cell subset we found that Arsenic exposure was also associated with a significant increase in the percentage of circulating proinflammatory Th17 cells. PAH exposure was associated with changes in T cells, monocytes and T memory (Tmem) cells and with changes in Th, Th1, Th2 and Th17 subsets all of which were non-monotonic (dose dependent). Alterations of immune cell populations caused by environmental exposures to As and PAH may result in adverse health outcomes, such as changes in systemic inflammation, immune suppression, or autoimmunity.

Citing Articles

Arsenic exposure is associated with alterations to multiple red blood cell parameters among adults in rural Bangladesh.

Medina S, Zhang Q, Lauer F, Santos-Medina L, Factor-Litvak P, Islam T Toxicol Appl Pharmacol. 2024; 484:116858.

PMID: 38341105 PMC: 11069126. DOI: 10.1016/j.taap.2024.116858.

Effect of polycyclic aromatic hydrocarbons on immunity.

Yu Y, Jin H, Lu Q J Transl Autoimmun. 2022; 5:100177.

PMID: 36561540 PMC: 9763510. DOI: 10.1016/j.jtauto.2022.100177.

Human Variation in DNA Repair, Immune Function, and Cancer Risk.

Cheong A, Nagel Z Front Immunol. 2022; 13:899574.

PMID: 35935942 PMC: 9354717. DOI: 10.3389/fimmu.2022.899574.

Exposure to arsenic and level of Vitamin D influence the number of Th17 cells and production of IL-17A in human peripheral blood mononuclear cells in adults.

Parvez F, Lauer F, Factor-Litvak P, Islam T, Eunus M, Horayara M PLoS One. 2022; 17(4):e0266168.

PMID: 35404942 PMC: 9000092. DOI: 10.1371/journal.pone.0266168.

Polycyclic Aromatic Hydrocarbons Affect Rheumatoid Arthritis Pathogenesis Aryl Hydrocarbon Receptor.

Xi X, Ye Q, Fan D, Cao X, Wang Q, Wang X Front Immunol. 2022; 13:797815.

PMID: 35392076 PMC: 8981517. DOI: 10.3389/fimmu.2022.797815.

References

Burchiel S, Luster M . Signaling by environmental polycyclic aromatic hydrocarbons in human lymphocytes. Clin Immunol. 2001; 98(1):2-10. DOI: 10.1006/clim.2000.4934. View

Maier A, Schumann B, Chang X, Talaska G, Puga A . Arsenic co-exposure potentiates benzo[a]pyrene genotoxicity. Mutat Res. 2002; 517(1-2):101-11. DOI: 10.1016/s1383-5718(02)00057-8. View

Gammon M, Santella R, Neugut A, Eng S, Teitelbaum S, Paykin A . Environmental toxins and breast cancer on Long Island. I. Polycyclic aromatic hydrocarbon DNA adducts. Cancer Epidemiol Biomarkers Prev. 2002; 11(8):677-85. View

Divi R, Beland F, Fu P, Von Tungeln L, Schoket B, Camara J . Highly sensitive chemiluminescence immunoassay for benzo[a]pyrene-DNA adducts: validation by comparison with other methods, and use in human biomonitoring. Carcinogenesis. 2003; 23(12):2043-9. DOI: 10.1093/carcin/23.12.2043. View

Rahman M, Arslan M, Chen Y, Ali S, Parvin T, Wang L . Polycyclic aromatic hydrocarbon-DNA adducts among rickshaw drivers in Dhaka City, Bangladesh. Int Arch Occup Environ Health. 2003; 76(7):533-8. DOI: 10.1007/s00420-003-0431-z. View

Karakaya A, Ates I, Yucesoy B . Effects of occupational polycyclic aromatic hydrocarbon exposure on T-lymphocyte functions and natural killer cell activity in asphalt and coke oven workers. Hum Exp Toxicol. 2004; 23(7):317-22. DOI: 10.1191/0960327104ht455oa. View

Soto-Pena G, Luna A, Acosta-Saavedra L, Conde P, Lopez-Carrillo L, Cebrian M . Assessment of lymphocyte subpopulations and cytokine secretion in children exposed to arsenic. FASEB J. 2006; 20(6):779-81. DOI: 10.1096/fj.05-4860fje. View

Lemarie A, Morzadec C, Bourdonnay E, Fardel O, Vernhet L . Human macrophages constitute targets for immunotoxic inorganic arsenic. J Immunol. 2006; 177(5):3019-27. DOI: 10.4049/jimmunol.177.5.3019. View

Mannino D, Buist A . Global burden of COPD: risk factors, prevalence, and future trends. Lancet. 2007; 370(9589):765-73. DOI: 10.1016/S0140-6736(07)61380-4. View

10.

Hertz-Picciotto I, Baker R, Yap P, Dostal M, Joad J, Lipsett M . Early childhood lower respiratory illness and air pollution. Environ Health Perspect. 2007; 115(10):1510-8. PMC: 2022654. DOI: 10.1289/ehp.9617. View

11.

Parvez F, Chen Y, Brandt-Rauf P, Bernard A, Dumont X, Slavkovich V . Nonmalignant respiratory effects of chronic arsenic exposure from drinking water among never-smokers in Bangladesh. Environ Health Perspect. 2008; 116(2):190-5. PMC: 2235213. DOI: 10.1289/ehp.9507. View

12.

Nixon D, Mussmann G, Eckdahl S, Moyer T . Total arsenic in urine: palladium-persulfate vs nickel as a matrix modifier for graphite furnace atomic absorption spectrophotometry. Clin Chem. 1991; 37(9):1575-9. View

13.

Ding W, Liu W, Cooper K, Qin X, de Souza Bergo P, Hudson L . Inhibition of poly(ADP-ribose) polymerase-1 by arsenite interferes with repair of oxidative DNA damage. J Biol Chem. 2008; 284(11):6809-17. PMC: 2652344. DOI: 10.1074/jbc.M805566200. View

14.

Pope 3rd C, Ezzati M, Dockery D . Fine-particulate air pollution and life expectancy in the United States. N Engl J Med. 2009; 360(4):376-86. PMC: 3382057. DOI: 10.1056/NEJMsa0805646. View

15.

Banerjee N, Banerjee S, Sen R, Bandyopadhyay A, Sarma N, Majumder P . Chronic arsenic exposure impairs macrophage functions in the exposed individuals. J Clin Immunol. 2009; 29(5):582-94. DOI: 10.1007/s10875-009-9304-x. View

16.

Kozul C, Hampton T, Davey J, Gosse J, Nomikos A, Eisenhauer P . Chronic exposure to arsenic in the drinking water alters the expression of immune response genes in mouse lung. Environ Health Perspect. 2009; 117(7):1108-15. PMC: 2717138. DOI: 10.1289/ehp.0800199. View

17.

Kozul C, Ely K, Enelow R, Hamilton J . Low-dose arsenic compromises the immune response to influenza A infection in vivo. Environ Health Perspect. 2009; 117(9):1441-7. PMC: 2737023. DOI: 10.1289/ehp.0900911. View

18.

Burchiel S, Mitchell L, Lauer F, Sun X, McDonald J, Hudson L . Immunotoxicity and biodistribution analysis of arsenic trioxide in C57Bl/6 mice following a 2-week inhalation exposure. Toxicol Appl Pharmacol. 2009; 241(3):253-9. PMC: 2843624. DOI: 10.1016/j.taap.2009.09.019. View

19.

Zhu J, Yamane H, Paul W . Differentiation of effector CD4 T cell populations (*). Annu Rev Immunol. 2010; 28:445-89. PMC: 3502616. DOI: 10.1146/annurev-immunol-030409-101212. View

20.

Li Q, Lauer F, Liu K, Hudson L, Burchiel S . Low-dose synergistic immunosuppression of T-dependent antibody responses by polycyclic aromatic hydrocarbons and arsenic in C57BL/6J murine spleen cells. Toxicol Appl Pharmacol. 2010; 245(3):344-51. PMC: 4271546. DOI: 10.1016/j.taap.2010.03.020. View