Bisphenol A exposure alters release of immune and developmental modulators and expression of estrogen receptors in human fetal lung fibroblasts

Journal of Environmental Sciences (China)

Volumn 48, Issue , 2016, Pages 11-23

  Mahemuti, Laziyan ^a,e   Chen, Qixuan ^a   Coughlan, Melanie C ^a   Zhang, Min ^a   Florian, Maria ^a,e   Mailloux, Ryan J ^a,e   Cao, Xu Liang ^b   Scoggan, Kylie A ^c,d   Willmore, William G ^e   Jin, Xiaolei ^a  

^a TOXICOLOGY RESEARCH DIVISION   (Canada)

^b FOOD RESEARCH DIVISION   (Canada)

^c Bureau of Nutritional Sciences   (Canada)

^d Environmental Health Center   (Canada)

^e CARLETON UNIVERSITY   (Canada)

Author keywords

Antagonists; Bisphenol A; Chemokines; Cytokines; Estrogen receptors; Human fetal lung fibroblasts; Immune and developmental modulators

Indexed keywords

AMINO ACIDS; BIOLOGICAL ORGANS; CELL CULTURE; DISEASES; FIBROBLASTS; PHENOLS;

ANTAGONISTS; BIS-PHENOL A; CHEMOKINES; CYTOKINES; ESTROGEN RECEPTOR; HUMAN FETAL LUNG FIBROBLAST;

PROTEINS;

ASTHMA; ENDOCRINE DISRUPTOR; GENE EXPRESSION; IMMUNE SYSTEM; PROTEIN;

4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; ENDOCRINE DISRUPTOR; ESTROGEN; ESTROGEN RECEPTOR; INTERLEUKIN 6; PHENOL DERIVATIVE;

CELL LINE; FIBROBLAST; HUMAN; METABOLISM;

BENZHYDRYL COMPOUNDS; CELL LINE; ENDOCRINE DISRUPTORS; ESTROGENS, NON-STEROIDAL; FIBROBLASTS; HUMANS; INTERLEUKIN-6; PHENOLS; RECEPTORS, ESTROGEN;

EID: 84969651446     PISSN: 10010742     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jes.2016.02.013     Document Type: Article

References (58)

1. Alkhouri, H., Poppinga, W.J., Tania, N.P., Ammit, A., Schuliga, M., Regulation of pulmonary inflammation by mesenchymal cells. Pulm. Pharmacol. Ther. 29:2 (2014), 156–165.
2. Asahi, J., Kamo, H., Baba, R., Doi, Y., Yamashita, A., Murakami, D. et al., Bisphenol A induces endoplasmic reticulum stress-associated apoptosis in mouse non-parenchymal hepatocytes. Life Sci. 87 (2010), 431–438.
3. Bauer, S.M., Roy, A., Emo, J., Chapman, T.J., Georas, S.N., Lawrence, B.P., The effects of maternal exposure to bisphenol a on allergic lung inflammation into adulthood. Toxicol. Sci. 130 (2012), 82–93.
4. Bonds, R.S., Midoro-Horiuti, T., Estrogen effects in allergy and asthma. Curr. Opin. Allergy Clin. Immunol. 13 (2013), 92–99.
5. Buteau-Lozano, H., Velasco, G., Cristofari, M., Balaguer, P., Perrot-Applanat, M., Xenoestrogens modulate vascular endothelial growth factor secretion in breast cancer cells through an estrogen receptor-dependent mechanism. J. Endocrinol. 196 (2008), 399–412.
6. Cao, X.L., Corriveau, J., Popovic, S., Coughlan, M.C., Chepelev, N., Willmore, W. et al., Background bisphenol A in experimental materials and its implication to low-dose in vitro study. Chemosphere 81:6 (2010), 817–820.
7. Cao, X.L., Zhang, J., Goodyer, C.G., Hayward, S., Cooke, G.M., Curran, I.H., Bisphenol A in human placental and fetal liver tissues collected from Greater Montreal area (Quebec) during 1998–2008. Chemosphere 89:5 (2012), 505–511.
8. Carroll, N.G., Mutavdzic, S., James, A.L., Distribution and degranulation of airway mast cells in normal and asthmatic subjects. Eur. Respir. J. 19 (2002), 879–885.
9. Chepelev, N.L., Enikanolaiye, M.I., Chepelev, L.L., Almohaisen, A., Chen, Q., Scoggan, K.A. et al., Bisphenol A activates the Nrf1/2-antioxidant response element pathway in HEK 293 cells. Chem. Res. Toxicol. 26 (2013), 498–506.
10. Dang, V.H., Choi, K.C., Hyun, S.H., Jeung, E.B., Induction of uterine calbindin-D9k through an estrogen receptor-dependent pathway following single injection with xenobiotic agents in immature rats. J. Toxicol. Environ. Health A 70 (2007), 171–182.
11. DiCosmo, B.F., Geba, G.P., Picarella, D., Elias, J.A., Rankin, J.A., Stripp, B.R. et al., Airway epithelial cell expression of interleukin-6 in transgenic mice. Uncoupling of airway inflammation and bronchial hyperreactivity. J. Clin. Invest. 94 (1994), 2028–2035.
12. Dijkstra, A., Howard, T.D., Vonk, J.M., Ampleford, E.J., Lange, L.A., Bleecker, E.R. et al., Estrogen receptor 1 polymorphisms are associated with airway hyperresponsiveness and lung function decline, particularly in female subjects with asthma. J. Allergy Clin. Immunol. 117 (2006), 604–611.
13. Durando, M., Kass, L., Piva, J., Sonnenschein, C., Soto, A.M., Luque, E.H. et al., Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ. Health Perspect. 115 (2007), 80–86.
14. Edlow, A.G., Chen, M., Smith, N.A., Lu, C., McElrath, T.F., Fetal bisphenol A exposure: concentration of conjugated and unconjugated bisphenol A in amniotic fluid in the second and third trimesters. Reprod. Toxicol. 34:1 (2012), 1–7.
15. Fixman, E.D., Stewart, A., Martin, J.G., Basic mechanisms of development of airway structural changes in asthma. Eur. Respir. J. 29 (2007), 379–389.
16. Folkman, J., Shing, Y., Angiogenesis. J. Biol. Chem. 267:16 (1992), 10931–10934.
17. Goldie, R.G.L., Fernandes, L.B., A possible mediator role for endothelin-1 in respiratory disease. Monaldi Arch. Chest Dis. 55 (2000), 162–167.
18. Golub, M.S., Wu, K.L., Kaufman, F.L., Li, L.H., Moran-Messen, F., Zeise, L. et al., Bisphenol A: developmental toxicity from early prenatal exposure. Birth Defects Res. B Dev. Reprod. Toxicol. 89:6 (2010), 441–466.
19. Gomez, R.F., Svanes, C., Macsali, F., Omenaas, R., Hormonal factors and respiratory health in women: a review. Clin. Respir. J. 2 (2008), 111–119.
20. Hanet, N., Lancon, A., Delmas, D., Jannin, B., Chagnon, M.C., Cherkaoui-Malki, M. et al., Effects of endocrine disruptors on genes associated with 17beta-estradiol metabolism and excretion. Steroids 73 (2008), 1242–1251.
21. Hijazi, A., Guan, H., Cernea, M., Yang, K., Prenatal exposure to bisphenol A disrupts mouse fetal lung development. FASEB J. 29:12 (2015), 4968–4977.
22. Hirst, S.J., Walker, T.R., Chilvers, E.R., Phenotypic diversity and molecular mechanisms of airway smooth muscle proliferation in asthma. Eur. Respir. J. 16 (2000), 159–177.
23. Hochrainer, K., Racchumi, G., Anrather, J., Site-specific phosphorylation of the p65 protein subunit mediates selective gene expression by differential NF-κB and RNA polymerase II promoter recruitment. Biol. Chem. 288:1 (2013), 285–293.
24. Hunt, P.A., Koehler, K.E., Susiarjo, M., Hodges, C.A., Ilagan, A., Voigt, R.C. et al., Bisphenol A exposure causes meiotic aneuploidy in the female mouse. Curr. Biol. 13 (2003), 546–553.
25. Ikezuki, Y., Tsutsumi, O., Takai, Y., Kamei, Y., Taketani, Y., Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum. Reprod. 17:11 (2002), 2839–2841.
26. Ivanova, M.M., Mazhawidza, W., Dougherty, S.M., Minna, J.D., Klinge, C.M., Activity and intracellular location of estrogen receptors a and b in human bronchial epithelial cells. Mol. Cell. Endocrinol. 305 (2009), 12–21.
27. Jobe, A.H., Ikegami, M., Antenatal infection/inflammation and postnatal lung maturation and injury. Respir. Res. 2 (2001), 27–32.
28. Kvingedal, A.M., Smeland, E.B., A novel putative G-protein-coupled receptor expressed in lung, heart and lymphoid tissue. FEBS Lett. 407 (1997), 59–62.
29. Lambrecht, S., Smith, V., De Wilde, K., Coudenys, J., Decuman, S., Deforce, D. et al., GDF15, a marker of lung involvement in systemic sclerosis, is involved in fibrosis development but does not impair fibrosis development. Arthritis Rheum. 66 (2014), 418–427.
30. Lim, R.H., Kobzik, L., Sexual tension in the airways. The puzzling duality of estrogen in asthma. Am. J. Respir. Cell Mol. Biol. 38 (2008), 499–500.
31. Massaro, D., Massaro, G.D., Estrogen receptor regulation of pulmonary alveolar dimensions: alveolar sex dimorphism in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 290 (2006), L866–L870.
32. McClintock, J.Y., Wagner, E.M., Role of IL-6 in systemic angiogenesis of the lung. J. Appl. Physiol. 99 (2005), 861–866.
33. Midoro-Horiuti, T., Tiwari, R., Watson, C.S., Goldblum, R.M., Maternal bisphenol a exposure promotes the development of experimental asthma in mouse pups. Environ. Health Perspect. 118 (2010), 273–277.
34. Miotto, D., Christodoulopoulos, P., Olivenstein, R., Taha, R., Cameron, L., Tsicopoulos, A. et al., Expression of IFN-gamma-inducible protein; monocyte chemotactic proteins 1, 3, and 4; and eotaxin in TH1- and TH2-mediated lung diseases. J. Allergy Clin. Immunol. 107 (2001), 664–670.
35. Nagase, T., Kurihara, H., Kurihara, Y., Aoki, T., Fukuchi, Y., Yazaki, Y. et al., Airway hyperresponsiveness to methacholine in mutant mice deficient in endothelin-1. Am. J. Respir. Crit. Care Med. 157 (1998), 560–564.
36. Nakajima, Y., Goldblum, R.M., Midoro-Horiuti, T., Fetal exposure to bisphenol A as a risk factor for the development of childhood asthma: an animal model study. Environ. Health, 11, 2012, 8.
37. Nogueira-Silva, C., Santos, M., Baptista, M.J., Moura, R.S., Correia-Pinto, J., IL-6 is constitutively expressed during lung morphogenesis and enhances fetal lung explant branching. Pediatr. Res. 60 (2006), 530–536.
38. Owman, C., Blay, P., Nilsson, C., Lolait, S.J., Cloning of human cDNA encoding a novel heptahelix receptor expressed in Burkitt's lymphoma and widely distributed in brain and peripheral tissues. Biochem. Biophys. Res. Commun. 228 (1996), 285–292.
39. Pain, M., Bermudez, O., Lacoste, P., Royer, P.J., Botturi, K., Tissot, A. et al., Tissue remodelling in chronic bronchial diseases: from the epithelial to mesenchymal phenotype. Eur. Respir. Rev. 23 (2014), 118–130.
40. Palanza, P., Gioiosa, L., vom Saal, F.S., Parmigiani, S., Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ. Res. 108 (2008), 150–157.
41. Pantano, C., Ather, J.L., Alcorn, J.F., Poynter, M.E., Brown, A.L., Guala, A.S. et al., Nuclear factor-κB activation in airway epithelium induces inflammation and hyperresponsiveness. Am. J. Respir. Crit. Care Med. 177 (2008), 959–969.
42. Robb, E.L., Stuart, J.A., The stilbenes resveratrol, pterostilbene and piceid affect growth and stress resistance in mammalian cells via a mechanism requiring estrogen receptor beta and the induction of Mn-superoxide dismutase. Phytochemistry 98 (2014), 164–173.
43. Schuliga, M., NF-kappaB signaling in chronic inflammatory airway disease. Biomolecules 5:3 (2015), 1266–1283.
44. Shimoya, K., Taniguchi, T., Matsuzaki, N., Moriyama, A., Murata, Y., Kitajima, H. et al., Chorioamnionitis decreased incidence of respiratory distress syndrome by elevating fetal interleukin-6 serum concentration. Hum. Reprod. 15 (2000), 2234–2240.
45. Sivakumar, P., Ntolios, P., Jenkins, G., Laurent, G., Into the matrix: targeting fibroblasts in pulmonary fibrosis. Curr. Opin. Pulm. Med. 18 (2012), 462–469.
46. Snijder, C.A., Pierik, F.H., Hofman, A., Jaddoe, V.W., Koch, H.M., Longnecker, M.P. et al., Fetal growth and prenatal exposure to bisphenol A: the generation R study. Environ. Health Perspect. 121 (2013), 393–398.
47. Spanier, A.J., Kahn, R.S., Kunselman, A.R., Prenatal exposure to bisphenol A and child wheeze from birth to 3 years of age. Environ. Health Perspect. 120:6 (2012), 916–920.
48. Takahashi, O., Oishi, S., Disposition of orally administered 2,2-Bis(4-hydroxyphenyl) propane (bisphenol A) in pregnant rats and the placental transfer to fetuses. Environ. Health Perspect. 108 (2000), 931–935.
49. Tharp, A.P., Maffini, M.V., Hunt, P.A., VandeVoort, C.A., Sonnenschein, C., Soto, A.M., Bisphenol A alters the development of the rhesus monkey mammary gland. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 8190–8195.
50. Ticconi, C., Pietropolli, A., Piccione, E., Estrogen replacement therapy and asthma. Pulm. Pharmacol. Ther. 26:6 (2013), 617–623.
51. Van Winkle, L.S., Murphy, S.R., Boetticher, M.V., VandeVoort, C.A., Fetal exposure of rhesus macaques to bisphenol A alters cellular development of the conducting airway by changing epithelial secretory product expression. Environ. Health Perspect. 121:8 (2013), 912–918.
52. Vandenberg, L.N., Maffini, M.V., Wadia, P.R., Sonnenschein, C., Rubin, B.S., Soto, A.M., Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 148 (2007), 116–127.
53. Vandenberg, L.N., Chahoud, I., Heindel, J.J., Padmanabhan, V., Paumgartten, F.J., Schoenfelder, G., Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol a. Cien. Saude Colet. 17:2 (2012), 407–434.
54. Vanhara, P., Lincova´, E., Kozubı'k, A., Jurdic, P., Soucek, K., Smarda, J., Growth/differentiation factor-15 inhibits differentiation into osteoclasts—a novel factor involved in control of osteoclast differentiation. Differentiation 78 (2009), 213–222.
55. Wang, J., Homer, R.J., Chen, Q., Elias, J.A., Endogenous and exogenous IL-6 inhibits aeroallergen-induced Th2 inflammation. J. Immunol. 165 (2000), 4051–4061.
56. WHO, GINA Report, Global Strategy for Asthma Management and Prevention. 2010, World Health Organization, Geneva, Swizerland.
57. Wu, Q., Jiang, D., Chu, H.W., Cigarette smoke induces growth differentiation factor 15 production in human lung epithelial cells: implication in mucin over-expression. Innate Immun. 18 (2012), 617–626.
58. Yoshitake, J., Kato, K., Yoshioka, D., Sueishi, Y., Sawa, T., Akaike, T. et al., Suppression of NO production and 8-nitroguanosine formation by phenol-containing endocrine-disrupting chemicals in LPS-stimulated macrophages: involvement of estrogen receptor-dependent or -independent pathways. Nitric Oxide 18 (2008), 223–228.