Mono(2-ethylhexyl) phthalate induces both pro- and anti-inflammatory responses in rat alveolar macrophages through crosstalk between p38, the lipoxygenase pathway and PPARα

References

• Anogianaki, A., Castellani, M. L., Madhappan, B., Salini, V., Vecchiet, J., Tete, S., Frydas, S., Perrella, A., De Lutiis, M. A., Neri, G., Cerulli, G., Caraffa, A., and Conti, P. 2008. RANTES (CCL5) potentiates calcium ionophore in the production of LTB4 in rat adherent macrophages from granuloma induced by KMnO4: Inhibition by NDGA. Pharmacol. Res. 57: 49–55.
   PubMed Web of Science ®Google Scholar
• Balashazy, I., Farkas, A., Szoke, I., Hofmann, W., and Sturm, R. 2003. Simulation of deposition and clearance of inhaled particles in central human airways. Radiat. Prot. Dosimetry. 105: 129–132.
   PubMed Web of Science ®Google Scholar
• Bernstein, D. I. 2008. ABCs of Asthma. Clin. Cornerstone. 8: 9–25.
   PubMedGoogle Scholar
• Bhattacharya, N., Dufour, J. M., Vo, M. N., Okita, J., Okita, R., and Kim, K. H. 2005. Differential effects of phthalates on the testis and the liver. Biol. Reprod. 72: 745–754.
   PubMed Web of Science ®Google Scholar
• Bonizzi, G., Piette, J., Schoonbroodt, S., Greimers, R., Havard, L., Merville, M. P., and Bours, V. 1999. Reactive oxygen intermediate-dependent NF-kappaB activation by interleukin-1beta requires 5-lipoxygenase or NADPH oxidase activity. Mol. Cell Biol. 19: 1950–1960.
   PubMed Web of Science ®Google Scholar
• Bornehag, C. G., Sundell, J., Weschler, C. J., Sigsgaard, T., Lundgren, B., Hasselgren, M., and Hagerhed-Engman, L. 2004. The association between asthma and allergic symptoms in children and phthalates in house dust: A nested case-control study. Environ. Health Perspect. 112: 1393–1397.
   PubMed Web of Science ®Google Scholar
• Bousquet, J., Jeffery, P. K., Busse, W. W., Johnson, M., and Vignola, A. M. 2000. Asthma. From bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care Med. 161: 1720–1745.
   PubMed Web of Science ®Google Scholar
• Boyce, J. A. 2008. Eicosanoids in asthma, allergic inflammation, and host defense. Curr. Mol. Med. 8: 335–349.
   PubMed Web of Science ®Google Scholar
• Cabrero, A., Laguna, J. C., and Vazquez, M. 2002. Peroxisome proliferator-activated receptors and the control of inflammation. Curr. Drug Targets. Inflamm. Allergy 1: 243–248.
   PubMedGoogle Scholar
• Carter, A. B., Monick, M. M., and Hunninghake, G. W. 1999. Both Erk and p38 kinases are necessary for cytokine gene transcription. Am. J. Respir. Cell Mol. Biol. 20: 751–758.
   PubMed Web of Science ®Google Scholar
• Carter, J. E., Roll, D. B., and Petersen, R. V. 1974. The in vitro hydrolysis of di-(2-ethylhexyl)phthalate by rat tissues. Drug Metab. Dispos. 2(4): 341–344.
   PubMed Web of Science ®Google Scholar
• Cernuda-Morollon, E., Rodriguez-Pascual, F., Klatt, P., Lamas, S., and Perez-Sala, D. 2002. PPAR agonists amplify iNOS expression while inhibiting NF-kappaB: Implications for mesangial cell activation by cytokines. J. Am. Soc. Nephrol. 13: 2223–2231.
   PubMed Web of Science ®Google Scholar
• Christie, P. E., and Barnes, N. C. 1996. Leukotriene B4 and asthma. Thorax. 51: 1171–1173.
   PubMed Web of Science ®Google Scholar
• Chung, K. F. 2005. Inflammatory mediators in chronic obstructive pulmonary disease. Curr. Drug Targets. Inflamm. Allergy. 4: 619–625.
   PubMedGoogle Scholar
• Coles, S. J., Neill, K. H., Reid, L. M., Austen, K. F., Nii, Y., Corey, E. J., and Lewis, R. A. 1983. Effects of leukotrienes C4 and D4 on glycoprotein and lysozyme secretion by human bronchial mucosa. Prostaglandins. 25: 155–170.
   PubMed Web of Science ®Google Scholar
• Crofford, L. J., Lipsky, P. E., Brooks, P., Abramson, S. B., Simon, L. S., and van de Putte, L. B. 2000. Basic biology and clinical application of specific cyclooxygenase-2 inhibitors. Arthritis Rheum. 43: 4–13.
   PubMed Web of Science ®Google Scholar
• Cuzzocrea, S., Mazzon, E., Di Paola R., Peli, A., Bonato, A., Britti, D., Genovese, T., Muia, C., Crisafulli, C., and Caputi, A. P. 2006. The role of the peroxisome proliferator-activated receptor-alpha (PPAR-alpha) in the regulation of acute inflammation. J. Leukocyte Biol. 79: 999–1010.
   PubMed Web of Science ®Google Scholar
• Delerive, P., De Bosscher K., Besnard, S., Vanden Berghe, W., Peters, J. M., Gonzalez, F. J., Fruchart, J. C., Tedgui, A., Haegeman, G., and Staels, B. 1999. Peroxisome proliferator-activated receptor alpha negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-kappaB and AP-1. J. Biol. Chem. 274: 32048–32054.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Dempsey, P. W., Doyle, S. E., He, J. Q., and Cheng, G. 2003. The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev. 14: 193–209.
   PubMed Web of Science ®Google Scholar
• Devchand, P. R., Keller, H., Peters, J. M., Vazquez, M., Gonzalez, F. J., and Wahli, W. 1996. The PPARalpha-leukotriene B4 pathway to inflammation control. Nature. 384: 39–43.
   PubMed Web of Science ®Google Scholar
• Dubois, C. M., Bissonnette, E., and Rola-Pleszczynski, M. 1989. Asbestos fibers and silica particles stimulate rat alveolar macrophages to release tumor necrosis factor. Autoregulatory role of leukotriene B4. Am. Rev. Respir. Dis. 139: 1257–1264.
   PubMed Web of Science ®Google Scholar
• Duty, S. M., Singh, N. P., Silva, M. J., Barr, D. B., Brock, J. W., Ryan, L., Herrick, R. F., Christiani, D. C., and Hauser, R. 2003. The relationship between environmental exposures to phthalates and DNA damage in human sperm using the neutral comet assay. Environ. Health Perspect. 111: 1164–1169.
   PubMed Web of Science ®Google Scholar
• European Chemicals Agency. 2008. Member state committee support document for identification of bis(2-ethylhexyl)phthalate (DEHP) as a substrate of very high concern. http://echa.europa.eu/doc/candidate_list/svhc_supdoc_dehp_publication.pdf
   Google Scholar
• Glue, C., Millner, A., Bodtger, U., Jinquan, T., and Poulsen, L. K. 2002. In vitro effects of monophthalates on cytokine expression in the monocytic cell line THP-1 and in peripheral blood mononuclear cells from allergic and non-allergic donors. Toxicol. In Vitro. 16: 657–662.
   PubMed Web of Science ®Google Scholar
• Hansen, J. S., Larsen, S. T., Poulsen, L. K., and Nielsen, G. D. 2007. Adjuvant effects of inhaled mono-2-ethylhexyl phthalate in BALB/cJ mice. Toxicology. 232: 79–88.
   PubMed Web of Science ®Google Scholar
• Hegen, M., Gaestel, M., Nickerson-Nutter, C. L., Lin, L. L., and Telliez, J. B. 2006. MAPKAP kinase 2-deficient mice are resistant to collagen-induced arthritis. J. Immunol. 177: 1913–1917.
   PubMed Web of Science ®Google Scholar
• Heudorf, U., Mersch-Sundermann, V., and Angerer, J. 2007. Phthalates: Toxicology and exposure. Int J Hyg. Environ. Health. 210: 623–634.
   PubMed Web of Science ®Google Scholar
• Im, J. Y., Kim, D., Lee, K. W., Kim, J. B., Lee, J. K., Kim, D. S., Lee, Y. I., Ha, K. S., Joe, C. O., and Han, P. L. 2004. COX-2 regulates the insulin-like growth factor I-induced potentiation of Zn(2+)-toxicity in primary cortical culture. Mol. Pharmacol.. 66: 368–376.
   PubMed Web of Science ®Google Scholar
• Jaakkola, J. J., and Knight, T. L. 2008. The role of exposure to phthalates from polyvinyl chloride products in the development of asthma and allergies: A systematic review and meta-analysis. Environ. Health Perspect. 116: 845–853.
   PubMed Web of Science ®Google Scholar
• Jepsen, K. F., Abildtrup, A., and Larsen, S. T. 2004. Monophthalates promote IL-6 and IL-8 production in the human epithelial cell line A549. Toxicol. In Vitro. 18: 265–269.
   PubMed Web of Science ®Google Scholar
• Jimenez, L. A., Drost, E. M., Gilmour, P. S., Rahman, I., Antonicelli, F., Ritchie, H., MacNee, W., and Donaldson, K. 2002. PM(10)-exposed macrophages stimulate a proinflammatory response in lung epithelial cells via TNF-alpha. Am. J. Physiol. Lung Cell Mol. Physiol. 282: L237–L248.
   PubMed Web of Science ®Google Scholar
• Kasahara, E., Sato, E. F., Miyoshi, M., Konaka, R., Hiramoto, K., Sasaki, J., Tokuda, M., Nakano, Y., and Inoue, M. 2002. Role of oxidative stress in germ cell apoptosis induced by di(2-ethylhexyl)phthalate. Biochem. J. 365: 849–856.
   PubMed Web of Science ®Google Scholar
• Kim, S. Y., Kim, T. B., Moon, K. A., Kim, T. J., Shin, D., Cho, Y. S., Moon, H. B., and Lee, K. Y. 2008. Regulation of pro-inflammatory responses by lipoxygenases via intracellular reactive oxygen species in vitro and in vivo. Exp. Mol. Med. 40: 461–476.
   PubMed Web of Science ®Google Scholar
• Koch, A., Giembycz, M., Ito, K., Lim, S., Jazrawi, E., Barnes, P. J., Adcock, I., Erdmann, E., and Chung, K. F. 2004a. Mitogen-activated protein kinase modulation of nuclear factor-kappaB-induced granulocyte macrophage-colony-stimulating factor release from human alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 30: 342–349.
   PubMed Web of Science ®Google Scholar
• Koch, A., Giembycz, M., Stirling, R. G., Lim, S., Adcock, I., Wassermann, K., Erdmann, E., and Chung, K. F. 2004b. Effect of smoking on MAP kinase-induced modulation of IL-8 in human alveolar macrophages. Eur. Respir. J. 23: 805–812.
   PubMed Web of Science ®Google Scholar
• Kusu, R., Oishi, A., Kakizawa, K., Kimura, T., Toda, C., Hashizume, K., Ueda, K., and Kojima, N. 2008. Effects of phthalate ester derivatives including oxidized metabolites on coactivator recruiting by PPARalpha and PPARgamma. Toxicol. In Vitro. 22: 1534–1538.
   PubMed Web of Science ®Google Scholar
• Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680–685.
   PubMed Web of Science ®Google Scholar
• Larsen, S. T., Hansen, J. S., Hansen, E. W., Clausen, P. A., and Nielsen, G. D. 2007. Airway inflammation and adjuvant effect after repeated airborne exposures to di-(2-ethylhexyl)phthalate and ovalbumin in BALB/c mice. Toxicology. 235: 119–129.
   PubMed Web of Science ®Google Scholar
• Ledwith, B. J., Pauley, C. J., Wagner, L. K., Rokos, C. L., Alberts, D. W., and Manam, S. 1997. Induction of cyclooxygenase-2 expression by peroxisome proliferators and non-tetradecanoylphorbol 12,13-myristate-type tumor promoters in immortalized mouse liver cells. J. Biol. Chem. 272: 3707–3714.
   PubMed Web of Science ®Google Scholar
• Lee, M. H., Park, J., Chung, S. W., Kang, B. Y., Kim, S. H., and Kim, T. S. 2004. Enhancement of interleukin-4 production in activated CD4+ T cells by diphthalate plasticizers via increased NF-AT binding activity. Int. Arch. Allergy Immunol. 134: 213–222.
   PubMed Web of Science ®Google Scholar
• Lefebvre, P., Chinetti, G., Fruchart, J. C., and Staels, B. 2006. Sorting out the roles of PPAR alpha in energy metabolism and vascular homeostasis. J. Clin. Invest. 116: 571–580.
   PubMed Web of Science ®Google Scholar
• Lentsch, A. B., and Ward, P. A. 2000. Regulation of inflammatory vascular damage. J. Pathol. 190: 343–348.
   PubMed Web of Science ®Google Scholar
• Lepley, R. A., and Fitzpatrick, F. A. 1998. 5-Lipoxygenase compartmentalization in granulocytic cells is modulated by an internal bipartite nuclear localizing sequence and nuclear factor kappa B complex formation. Arch. Biochem. Biophys. 356: 71–76.
   PubMed Web of Science ®Google Scholar
• Lovekamp-Swan, T., Jetten, A. M., and Davis, B. J. 2003. Dual activation of PPARalpha and PPARgamma by mono-(2-ethylhexyl) phthalate in rat ovarian granulosa cells. Mol. Cell Endocrinol. 201: 133–141.
   PubMed Web of Science ®Google Scholar
• Lu, J., Yang, Z., Jiang, J., Wang, Z., and Zhu, P. 2001. Regulative effect of P38MAPK on release of TNFalpha and NO from alveolar macrophages under endotoxin stimulation. Chin. J. Traumatol. 4: 75–77.
   PubMedGoogle Scholar
• Maloney, E. K., and Waxman, D. J. 1999. trans-Activation of PPARalpha and PPARgamma by structurally diverse environmental chemicals. Toxicol. Appl. Pharmacol. 161: 209–218.
   PubMed Web of Science ®Google Scholar
• Mandard, S., Muller, M., and Kersten, S. 2004. Peroxisome proliferator-activated receptor alpha target genes. Cell Mol. Life Sci. 61: 393–416.
   PubMed Web of Science ®Google Scholar
• McBride, W. H., Economou, J. S., Nayersina, R., Comora, S., and Essner, R. 1990. Influences of interleukins 2 and 4 on tumor necrosis factor production by murine mononuclear phagocytes. Cancer Res. 50: 2949–2952.
   PubMed Web of Science ®Google Scholar
• Moore, M. L., and Peebles, R. S. Jr. 2006. Update on the role of prostaglandins in allergic lung inflammation: separating friends from foes, harder than you might think. J. Allergy Clin. Immunol. 117: 1036–1039.
   PubMed Web of Science ®Google Scholar
• Nacife, V. P., Soeiro, M. N., Gomes, R. N., D’Avila, H., Castro-Faria Neto, H. C., and Meirelles, M. N. 2004. Morphological and biochemical characterization of macrophages activated by carrageenan and lipopolysaccharide in vivo. Cell Struct. Funct. 29: 27–34.
   PubMed Web of Science ®Google Scholar
• Nakamiya, K., Takagi, H., Nakayama, T., Ito, H., Tsuruga, H., Edmonds, J. S., and Morita, M. 2005. Microbial production and vaporization of mono-(2-ethylhexyl) phthalate from di-(2-ethylhexyl) phthalate by microorganisms inside houses. Arch. Environ. Occup. Health. 60: 321–325.
   PubMed Web of Science ®Google Scholar
• Nicosia, S., Capra, V., and Rovati, G. E. 2001. Leukotrienes as mediators of asthma. Pulm. Pharmacol. Ther. 14: 3–19.
   PubMed Web of Science ®Google Scholar
• Okamoto, H., Iwamoto, T., Kotake, S., Momohara, S., Yamanaka, H., and Kamatani, N. 2005. Inhibition of NF-kappaB signaling by fenofibrate, a peroxisome proliferator-activated receptor-alpha ligand, presents a therapeutic strategy for rheumatoid arthritis. Clin. Exp. Rheumatol. 23: 323–330.
   PubMed Web of Science ®Google Scholar
• Pant, N., Shukla, M., Kumar, P. D., Shukla, Y., Mathur, N., Kumar, G. Y., and Saxena, D. K. 2008. Correlation of phthalate exposures with semen quality. Toxicol. Appl. Pharmacol. 231: 112–116.
   PubMed Web of Science ®Google Scholar
• Parmar, D., Srivastava, S. P., Singh, G. B., and Seth, P. K. 1995. Testicular toxicity of di(2-ethylhexyl)phthalate in developing rats. Vet. Hum. Toxicol. 37: 310–313.
   PubMedGoogle Scholar
• Pascual, G., and Glass, C. K. 2006. Nuclear receptors versus inflammation: Mechanisms of transrepression. Trends Endocrinol. Metab. 17: 321–327.
   PubMed Web of Science ®Google Scholar
• Peck, C. C., and Albro, P. W. 1982. Toxic potential of the plasticizer di(2-ethylhexyl) phthalate in the context of its disposition and metabolism in primates and man. Environ. Health Perspect.45: 11–17.
   Web of Science ®Google Scholar
• Pereira, C., Mapuskar, K., and Rao, C. V. 2006. Chronic toxicity of diethyl phthalate in male Wistar rats—A dose-response study. Regul. Toxicol. Pharmacol. 45: 169–177.
   PubMed Web of Science ®Google Scholar
• Peters-Golden, M. 2004. The alveolar macrophage: The forgotten cell in asthma. Am. J. Respir. Cell Mol. Biol. 31: 3–7.
   PubMed Web of Science ®Google Scholar
• Rachelefsky, G. 1997. Childhood asthma and allergic rhinitis: The role of leukotrienes. J. Pediatr.131: 348–355.
   Google Scholar
• Rakkestad, K. E., Dye, C. J., Yttri, K. E., Holme, J. A., Hongslo, J. K., Schwarze, P. E., and Becher, R. 2007. Phthalate levels in Norwegian indoor air related to particle size fraction. J. Environ. Monit. 9: 1419–1425.
   PubMed Web of Science ®Google Scholar
• Raman, M., Chen, W., and Cobb, M. H. 2007. Differential regulation and properties of MAPKs. Oncogene. 26: 3100–3112.
   PubMed Web of Science ®Google Scholar
• Rao, K. M., Meighan, T., and Bowman, L. 2002. Role of mitogen-activated protein kinase activation in the production of inflammatory mediators: Differences between primary rat alveolar macrophages and macrophage cell lines. J. Toxicol. Environ. Health A. 65: 757–768.
   PubMed Web of Science ®Google Scholar
• Simeonova, P. P., Toriumi, W., Kommineni, C., Erkan, M., Munson, A. E., Rom, W. N., and Luster, M. I. 1997. Molecular regulation of IL-6 activation by asbestos in lung epithelial cells: Role of reactive oxygen species. J. Immunol.159: 3921–3928.
   Google Scholar
• Soberman, R. J., and Christmas, P. 2003. The organization and consequences of eicosanoid signaling. J. Clin. Invest. 111: 1107–1113.
   PubMed Web of Science ®Google Scholar
• Staels, B., Koenig, W., Habib, A., Merval, R., Lebret, M., Torra, I. P., Delerive, P., Fadel, A., Chinetti, G., Fruchart, J. C., Najib, J., Maclouf, J., and Tedgui, A. 1998. Activation of human aortic smooth-muscle cells is inhibited by PPARalpha but not by PPARgamma activators. Nature. 393: 790–793.
   PubMed Web of Science ®Google Scholar
• Standiford, T. J., Strieter, R. M., Chensue, S. W., Westwick, J., Kasahara, K., and Kunkel, S. L. 1990. IL-4 inhibits the expression of IL-8 from stimulated human monocytes. J. Immunol. 145: 1435–1439.
   PubMed Web of Science ®Google Scholar
• Stein, M., Keshav, S., Harris, N., and Gordon, S. 1992. Interleukin 4 potently enhances murine macrophage mannose receptor activity: A marker of alternative immunologic macrophage activation. J Exp. Med. 176: 287–292.
   PubMed Web of Science ®Google Scholar
• Stringer, B., and Kobzik, L. 1998. Environmental particulate-mediated cytokine production in lung epithelial cells (A549): Role of preexisting inflammation and oxidant stress. J. Toxicol. Environ. Health A.55: 31–44.
   PubMed Web of Science ®Google Scholar
• Surewicz, K., Aung, H., Kanost, R. A., Jones, L., Hejal, R., and Toossi, Z. 2004. The differential interaction of p38 MAP kinase and tumor necrosis factor-alpha in human alveolar macrophages and monocytes induced by Mycobacterium tuberculois. Cell Immunol. 228: 34–41.
   PubMed Web of Science ®Google Scholar
• Torres, M., and Forman, H. J. 1999. Activation of several MAP kinases upon stimulation of rat alveolar macrophages: Role of the NADPH oxidase. Arch. Biochem. Biophys. 366: 231–239.
   PubMed Web of Science ®Google Scholar
• Towbin, H., Staehelin, T., and Gordon, J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA. 76: 4350–4354.
   PubMed Web of Science ®Google Scholar
• Venkata, N. G., Robinson, J. A., Cabot, P. J., Davis, B., Monteith, G. R., and Roberts-Thomson, S. J. 2006. Mono(2-ethylhexyl)phthalate and mono-n-butyl phthalate activation of peroxisome proliferator activated-receptors alpha and gamma in breast. Toxicol. Lett. 163: 224–234.
   PubMed Web of Science ®Google Scholar
• Ward, P. A. 2003. Acute lung injury: How the lung inflammatory response works. Eur. Respir. J. Suppl. 44: 22s–23s.
   PubMedGoogle Scholar
• Werz, O., Klemm, J., Samuelsson, B., and Radmark, O. 2000. 5-Lipoxygenase is phosphorylated by p38 kinase-dependent MAPKAP kinases. Proc. Natl. Acad. Sci. USA. 97: 5261–5266.
   PubMed Web of Science ®Google Scholar
• Yao, P. L., Lin, Y. C., Sawhney, P., and Richburg, J. H. 2007. Transcriptional regulation of FasL expression and participation of sTNF-alpha in response to sertoli cell injury. J. Biol. Chem. 282: 5420–5431.
   PubMed Web of Science ®Google Scholar
• Yokoyama, Y., Okubo, T., Kano, I., Sato, S., and Kano, K. 2003. Induction of apoptosis by mono(2-ethylhexyl)phthalate (MEHP) in U937 cells. Toxicol. Lett. 144: 371–381.
   PubMed Web of Science ®Google Scholar