Immunotoxic effects of perfluorononanoic acid on BALB/c mice

Toxicological Sciences

Volumn 105, Issue 2, 2008, Pages 312-321

  Fang, Xuemei ^a,b   Zhang, Lianjun ^a   Feng, Yixing ^a   Zhao, Yong ^a   Dai, Jiayin ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Glucocorticoid; Immunotoxicity; NF B; PFNA; PPAR

Indexed keywords

ALPHA2 INTEGRIN; CONCANAVALIN A; CORTICOTROPIN; GAMMA INTERFERON; GLUCOCORTICOID RECEPTOR; GLYCOPROTEIN P 15095; HYDROCORTISONE; I KAPPA B ALPHA; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 4; PERFLUORO COMPOUND; PERFLUORONONANOIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CYCLE ARREST; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; CYTOKINE PRODUCTION; EXPOSURE; HOMEOSTASIS; HYDROCORTISONE BLOOD LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOTOXICITY; LYMPHOCYTE TRANSFORMATION; LYMPHOID ORGAN; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SPLEEN; THYMOCYTE; THYMUS; UPREGULATION; WEIGHT REDUCTION;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; ANTIGENS, CD; APOPTOSIS; BODY WEIGHT; CELL CYCLE; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; FLUOROCARBONS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNITY, CELLULAR; IMMUNITY, NATURAL; INTERFERON TYPE II; INTERLEUKIN-1BETA; INTERLEUKIN-4; MALE; MICE; MICE, INBRED BALB C; NF-KAPPA B; PITUITARY-ADRENAL SYSTEM; PPAR ALPHA; PPAR GAMMA; RNA, MESSENGER; SPLEEN; T-LYMPHOCYTES; THYMUS GLAND; TIME FACTORS;

MUS;

EID: 51849166078     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn127     Document Type: Article

References (53)

1. Abbott, B. D., Wolf, C. J., Schmid, J. E., Das, K. P., Zehr, R. D., Helfant, L., Nakayama, S., Lindstrom, A. B., Strynar, M. J., and Lau, C. (2007). Perfluorooctanoic acid induced developmental toxi city in the mouse is dependent on expression of peroxisome proliferator activated receptor-alpha. Toxicol. Sci. 98, 571-581.
2. Almawi, W. Y., and Melemedjian, O. K. (2002). Negative regulation of nuclear factor-kappaB activation and function by glucocorticoids. J. Mol. Endocrinol. 28, 69-78.
3. Baeuerle, P. A., and Baltimore, D. (1996). NF-kappa B: Ten years after. Cell 87, 13-20.
4. Bhat, M. S., Rao, G., Murthy, K. D., and Bhat, P. G. (2007). Housing in pyramid counteracts neuroendocrine and oxidative stress caused by chronic restraint in rats. Evid. Based Complement Alternat. Med. 4, 35-42.
5. Bishayi, B., and Ghosh, S. (2007). Immunobiological changes of in vivo glucocorticoid depleted male Swiss albino rats. Immunobiology 212, 19-27.
6. Boldizsár, F., Pálinkás, L., Czömpöly, T., Barris, D., Németh, P., and Berki, T. (2006). Low glucocorticoid receptor (GR), high Dig2 and low Bcl-2 expression. in double positive thymocytes of BALB/c, mice indicates their endogenous glucocorticoid hormone exposure. Immunobiology 211, 185-796.
7. Chen, X., Li, M., Sun, W., Bi, Y., Cai, M., Liang, H., Yu., Q., He, X., and Weng, J. (2008). Peroxisome proliferator-activated receptor alpha agonist-induced down-regulation of hepatic glucocorticoid receptor expression in SD rats. Biochem. Biophys. Res. Commun. 368, 865-870.
8. + T cells by peroxisome proliferator-activated receptor-gamma (PPAR-gamma) ligands: Involvement of physical association between PPAR-gamma and the nuclear factor of activated T cells transcription factor. Mol. Pharmacol. 64, 1169-1179.
9. Cunard, R., DiCampli, D., Archer, D. C., Stevenson, J. L., Ricote, M., Glass, C. K., and Kelly, C. J. (2002b). WY14,643, a PPAR alpha ligand, has profound effects on immune responses in vivo. J. Immunol. 169, 6806-6812.
10. Cunard, R., Eto, Y., Muljadi, J. T., Glass, C. K., Kelly, C. J., and Ricote, M. (2004). Repression of IFN-gamma expression by peroxisome proliferator-activated receptor gamma. J. Immunol. 172, 7530-7536.
11. Cunard, R., Ricote, M., DiCampli, D., Archer, D. C., Kahn, D. A., Glass, C. K., and Kelly, C. J. (2002a). Regulation of cytokine expression by ligands of peroxisome proliferator activated receptors. J. Immunol. 168, 2795-2802.
12. Dehmer, T., Heneka, M. T., Sastre, M., Dichgans, J., and Schulz, J. B. (2004). Protection by pioglitazone in the MPTP model of Parkinson's disease correlates with I kappa B alpha induction and block of NF kappa B and iNOS activation. J. Neurochem. 88, 494-501.
13. Delerive, P., Gervois, P., Fruchart, J. C., and Staels, B. (2000). Induction of IkappaBalpha expression as a mechanism contributing to the anti-inflammatory activities of peroxisome proliferator-activated receptor-alpha activators. J. Biol. Chem. 275, 36703-36707.
14. DeWitt, J. C., Copeland, C. B., Strynar, M. J., and Luebke, R. W. (2009). Perfluorooctanoic acid induced immunomodulation in adult C57BL/ 6J or C57BL/6N female mice. Environ. Health Perspect. 116, 644-650.
15. Elftman, M. D., Norbury, C. C., Bonneau, R. H., and Truckenmiller, M. E. (2007). Corticosterone impairs dendritic cell maturation and function. Immunology 122, 279-290.
16. Ellis, D. A., Martin, J. W., De Silva, A. O., Mabury, S. A., Hurley, M. D., Andersen, M. P. S., and Wallington, T. J. (2004). Degradation of fluorotelomer alcohol; A likely atmospheric source of perfluorinated carboxylic acids. Environ. Sci. Technol. 38, 3316-3321.
17. Giesy, J. P., and Karman, K. (2002). Perfluorochemical surfactants in the environment. Environ. Sci. Technol. 36, 146A-152A.
18. Guruge, K. S., Taniyasu, S., Yamashita, N., Wijeratna, S., Mohotti, K. M., Seneviratne, H. R., Kannan, K., Yamanaka, N., and Miyazaki, S. (2005). Perfluorinated organic compounds in human blood serum and seminal plasma: A study of urban and rural tea worker populations in Sri Lanka. J. Environ. Monit. 7, 371-377.
19. Haukas, M., Berger, U., Hop, H., Gulliksen, B., and Gabrielsen, G. W. (2007). Bioaccumulation of per- and polyfluorinated alkyl substances (PFAS) in selected species from the Barents Sea food web. Environ. Pollut. 148, 360-371.
20. Houde, M., Martin, J. W., Letcher, R. J., Solomon, K. R., and Muir, D. C. (2006). Biological monitoring of polyfluoroalkyl substances: A review. Environ. Sci. Technol. 40, 3463-3473.
21. Ialenti, A., Grassia, G., Di Meglio, P., Maffia, P., Di Rosa, M., and Ianaro, A. (2005). Mechanism of the anti-inflammatory effect of thiazolidinediones: Relationship with the glucocorticoid pathway. Mol. Pharmacol. 67, 1620-1628.
22. Jondal, M., Pazirandeh, A., and Okret, S. (2004). Different roles for glucocorticoids in thymocyte homeostasis? Trends. Immunol. 25 595-600.
23. Kleszczyński, K., Gardzielewski, P., Mulkiewicz, E., Stepnowski, P., and Składanowski, A. C. (2007). Analysis of structure-cytotoxicity in vitro relationship (SAR) for perfluorinated carboxylic acids. Toxicol. In Vitro 21, 1206-1211.
24. Kudo, N., Suzuki-Nakajima, E., Mitsumoto, A., and Kawashima, Y. (2006). Responses of the liver to perfluorinated fatty acids with different carbon chain length in male and female mice: In relation to induction of hepatomegaly, peroxisomal beta-oxidation and microsomal 1-acylglycerophosphocholine acyltransferase. Biol. Pharm. Bull. 29, 1952-1957.
25. Lau, C., Anitole, K., Hodes, C., Lai, D., Pfahles-Hutchens, A., and Seed, J. (2007). Perfluoroalkyl acids: A review of monitoring and toxicological findings. Toxicol. Sci. 99, 366-394.
26. Liberman, A. C., Druker, J., Perone, M. J., and Arzt, E. (2007). Glucocorticoids in the regulation of transcription factors that control cytokine synthesis. Cytokine Growth Factor Rev. 18, 45-56.
27. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25, 402-408.
28. Love, O. P., Shutt, L. J., Silfies, J. S., Bortolotti, G. R., Smits, J. E., and Bird, D. M. (2003). Effects of dietary PCB exposure on adrenocortical function in captive American kestrels (Falco sparverius). Ecotoxicology 12, 199-208.
29. Lovett-Racke, A. E., Hussain, R. Z., Northrop, S., Choy, J., Rocchini, A., Matthes, L., Chavis, J. A., Diab, A., Drew, P. D., and Racke, M. K. (2004). Peroxisome proliferator-activated receptor alpha agonists as therapy for autoimmune disease. J. Immunol. 172, 5790-5798.
30. Maloney, E. K., and Waxman, D. J. (1999). Trans-activation of PPARα and PPARγ by structurally diverse environmental chemicals. Toxicol. Appl. Pharmacol 161, 209-218.
31. Migliorati, G., Nicoletti, I., Nocentini, G., Pagliacci, M. C., and Riccardi, C. (1994). Dexamethasone and interleukins modulate apoptosis of murine thymocytes and peripheral T-lymphocytes. Pharmacology 30, 43-52.
32. Nakano, Y. (2007). Effect of chronic topical exposure to low-dose noxious chemicals and stress on skin sensitivity in mice. J. Occup. Health 49, 431-442.
33. Nelson, D. L., Frazier, D. E., Ericson, J. E., Tarr, M. J., and Mathes, L. E. (1992). The effects of perfluorodecanoic acid (PFDA) on humoral, cellular, and innate immunity in Fischer 344 rats. Immunopharmacol. Immunotoxicol 14, 925-938.
34. Pabello, N. G., and Lawrence, D. A. (2006). Neuroimmotoxicology: Modulation of neuroimmune networks by toxicants. Clin. Neurosci. Res. 6, 69-85.
35. Peden-Adams, M. M., EuDaly, J. G., Dabra, S., EuDaly, A., Heesemann, L., Smythe, J., and Keil, D. E. (2007). Suppression of humoral immunity following exposure to-the perfluorinated insecticide sulfluramid. J. Toxicol. Environ. Health A. 70, 1130-1141.
36. Peden-Adams, M. M., Keller, J. M., Eudaly, J. G., Berger, J., Gilkeson, G. S., and Keil, D. E. (2008). Suppression of humoral immunity in mice following exposure to perfluorooctane sulfonate (PFOS). Toxicol. Sci. doi:10.1093/toxsci/kfn059.
37. Preil, J., Müller, M. B., Gesing, A., Reul, J. M., Sillaber, I., van Gaalen, M. M., Landgrebe, J., Holsboer, F., Stenzel-Poore, M., and Wurst, W. (2001). Regulation of the hypothalamic-pituitary-adrenocortical system in mice deficient for CRH receptors 1 and 2. Endocrinology 142, 4946-4955.
38. Pruett, S. B., Collier, S., Wu, W. J., and Fan, R. (1999). Quantitative relationships between the suppression of selected immunological parameters and the area under the corticosterone concentration vs. time curve in B6C3F1 mice subjected to exogenous corticosterone or to restraint stress. Toxicol. Sci. 49, 272-280.
39. Reisman, D., and Thompson, E. A. (1995). Glucocorticoid regulation of cyclin D3 gene transcription and mRNA stability in lymphoid cells. Mol. Endocrinol. 9, 1500-1509.
40. Rice, D. C., and Hayward, S. (1997). Effects of postnatal-exposure to a PCB mixture in monkeys on nonspatial discrimination reversal and delayed alternation performance. Neurotoxicology 18, 479-494.
41. Ricote, M., Li, A. C., Willson, T. M., Kelly C. J., and Glass, C. K. (1998). The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 391, 79-82.
42. Scheinman, R. I., Cogswell, P. C., Lofquist, A. K., and Baldwin, A. S. (1995). Role of transcriptional activation of I kappa B alpha in mediation of immunosuppression by glucocorticoids. Science 270 283-286.
43. Shridhar, S., Farley, A., Reid, R. L., Foster, W. G., and Van Vugt, D. A. (2001). The effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on corticotrophin-releasing hormone, arginine vasopressin, and pro-opiomelanocortin mRNA levels in the hypothalamus of the cynomolgus monkey. Toxicol. Sci. 63, 181-188.
44. Smoak, K. A., and Cidlowski, J. A. (2004). Mechanisms of glucocorticoid receptor signaling during inflammation. Mech. Ageing. Dev. 125 697-706.
45. Song, C. (2005). n-3 Fatty acid EPA alone or in combination with GLA modulate BPA axis activity, inflammation condition, and related gene expressions in a rodent model of depression. Brain Behav. Immun. 19, e43-e74; e66.
46. Sung, B., Park, S., Yu, B. P., and Chung, H. Y. (2006). Amelioration of age-related inflammation and oxidative stress by PPARgamma activator: Suppression of NF-kappaB by 2,4-thiazolidinedione. Exp. Gerontol. 41, 590-599.
47. Tugwood, J. D., Issemann, L, Anderson, R. G., Bundell, K. R., McPheat, W. L., and Green, S. (1992). The mouse peroxisome proliferator activated receptor recognizes a response element in the 5′ flanking sequence of the rat acyl CoA oxidase gene. EMBO J. 11, 433-439.
48. Vanden Heuvel, J. P., Thompson, J. T., Frame, S. R., and Gillies, P. J. (2006). Differential activation of nuclear receptors by perfluorinated fatty acid analogs and natural fatty acids: A comparison of human, mouse, and rat peroxisome proliferator-activated receptoralpha, -beta, and -gamma, liver X receptor-beta, and retinoid X receptor-alpha. Toxicol. Sci. 92, 476-489.
49. Van de Vijver, K. I., Hoff, P., Das, K., Brasseur, S., Van Dongen, W., Esmans, E., Reijnders, P., Blust, R., and De Coen, W. (2005). Tissue distribution of perfluorinated chemicals in harbor seals (Phoca vitulina) from the Dutch Wadden Sea. Environ. Sci. Technol. 39, 6978-6984.
50. Yang, Q., Xie, Y., Alexson, S. E., Nelson, B. D., and DePierre, J. W. (2002). Involvement of the peroxisome proliferator-activated receptor alpha in the immunomodulation caused by peroxisome proliferators in mice. Biochem. Pharmacol. 63, 1893-1900.
51. Yang, Q., Xie, Y., and DePierre, J. W. (2000). Effects of peroxisome proliferators on the thymus and spleen of mice. Clin. Exp. Immunol. 122, 219-226.
52. Yang, Q., Xie, Y., Eriksson, A. M., Nelson, R. D., and DePierre, J. W. (2001). Further evidence for the involvement of inhibition of cell proliferation and development in thymic and splenic atrophy induced by the peroxisome proliferator perfluoroctanoic acid in mice. Biochem. Pharmacol. 62, 1133-1140.
53. Zhang, H., Shi, Z., Liu, Y., Wei, Y., and Dai, J. (2008). Lipid homeostasis and oxidative stress in the liver of male rats exposed to perfluorododecanoic acid. Toxicol. Appl. Pharmacol. 227, 16-25.