Maternal allergy acts synergistically with cigarette smoke exposure during pregnancy to induce hepatic fibrosis in adult male offspring

References

• Andersen, A. M. and Osler, M. 2004. Birth dimensions, parental mortality, and mortality in early adult age: A cohort study of Danish men born in 1953. Int. J. Epidemiol. 33:92–99.
   PubMedGoogle Scholar
• Bracken, M. B.,Triche, E. W., Belanger, K., Saftlas, A., Beckett, W. S. and Leaderer, B. P. 2003. Asthma symptoms, severity, and drug therapy: A prospective study of effects on 2205 pregnancies. Obstet. Gynecol. 102:739–752.
   PubMed Web of Science ®Google Scholar
• Clifton, V. L., Giles, W. B., Smith, R., Bisits, A. T., Hempenstall, P. A., Kessell, C. G. and Gibson, P. G. 2001. Alterations of placental vascular function in asthmatic pregnancies. Am. J. Respir. Crit. Care Med. 164:546–553.
   PubMed Web of Science ®Google Scholar
• Clifton, V. L., Hodyl, N. A., Murphy, V. E., Giles, W. B., Baxter, R. C. and Smith, R. 2010. Effect of maternal asthma, inhaled glucocorticoids and cigarette use during pregnancy on the newborn insulin-like growth factor axis. Growth Horm. IGF Res. 20:39–48.
   PubMed Web of Science ®Google Scholar
• Costenbader, K. H. and Karlson, E. W. 2006. Cigarette smoking and autoimmune disease: What can we learn from epidemiology? Lupus 15:737–745.
   PubMed Web of Science ®Google Scholar
• Cousins, L. 1999. Fetal oxygenation, assessment of fetal well-being, and obstetric management of the pregnant patient with asthma. J. Allergy Clin. Immunol. 103:S343–S349.
   PubMed Web of Science ®Google Scholar
• Dev, A., Patel, K., Conrad, A., Blatt, L. M. and McHutchison, J. G. 2006. Relationship of smoking and fibrosis in patients with chronic hepatitis C. Clin. Gastroenterol. Hepatol. 4:797–801.
   PubMed Web of Science ®Google Scholar
• Di Martino, V., Lebray, P., Myers, R. P., Pannier, E., Paradis, V., Charlotte, F., Moussalli, J., Thabut, D., Buffet, C. and Poynard, T. 2004. Progression of liver fibrosis in women infected with hepatitis C: Long-term benefit of estrogen exposure. Hepatology 40:1426–1433.
   PubMed Web of Science ®Google Scholar
• Diehl, A. M. 2004. Fatty liver, hypertension, and the metabolic syndrome. Gut 53:923–924.
   PubMed Web of Science ®Google Scholar
• Fedulov, A. V. and Kobzik, L. 2008. Immunotoxicologic analysis of maternal transmission of asthma risk. J. Immunotoxicol. 5:445–452.
   PubMed Web of Science ®Google Scholar
• Fleming, R. E., Britton, R. S., Waheed, A., Sly, W. S. and Bacon, B. R. 2004. Pathogenesis of hereditary hemochromatosis. Clin. Liver Dis. 8:755–773, vii.
   PubMedGoogle Scholar
• Fraser, A., Ebrahim, S., Smith, G. D. and Lawlor, D. A. 2008. The associations between birthweight and adult markers of liver damage and function. Paediatr. Perinat. Epidemiol. 22:12–21.
   PubMedGoogle Scholar
• Friedman, S. L. 2008. Mechanisms of hepatic fibrogenesis. Gastroenterology 134:1655–1669.
   PubMed Web of Science ®Google Scholar
• Gao, C., Miyazaki, M., Kondo, T., Tsuji, T., Sakaguchi, M. and Namba, M. 2001. Over-expression of platelet-derived growth factor B and down-regulation of PDGF-receptor α in human immortalized fibroblasts. Int. J. Oncol. 18:871–875.
   PubMedGoogle Scholar
• Horani, A., Muhanna, N., Pappo, O., Melhem, A., Alvarez, C. E., Doron, S., Wehbi, W., Dimitrios, K., Friedman, S. L. and Safadi, R. 2007. Beneficial effect of glatiramer acetate (Copaxone) on immune modulation of experimental hepatic fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G628–G638.
   Google Scholar
• Izzotti, A., Balansky, R. M., Cartiglia, C., Camoirano, A., Longobardi, M. and De Flora, S. 2003. Genomic and transcriptional alterations in mouse fetus liver after transplacental exposure to cigarette smoke. FASEB J. 17:1127–1129.
   PubMed Web of Science ®Google Scholar
• Klatsky, A. L. and Armstrong, M. A. 1992. Alcohol, smoking, coffee, and cirrhosis. Am. J. Epidemiol. 136:1248–1257.
   PubMed Web of Science ®Google Scholar
• Lawlor, D. A., Najman, J. M., Sterne, J., Williams, G. M., Ebrahim, S. and Davey Smith, G. 2004. Associations of parental, birth, and early life characteristics with systolic blood pressure at 5 years of age: Findings from the Mater-University study of pregnancy and its outcomes. Circulation 110:2417–2423.
   PubMedGoogle Scholar
• Lefkowitch, J. H. 2007. Liver biopsy assessment in chronic hepatitis. Arch. Med. Res. 38:634–643.
   PubMedGoogle Scholar
• Lim, R. H. and Kobzik, L. 2009. Maternal transmission of asthma risk. Am. J. Reprod. Immunol. 61:1–10.
   PubMed Web of Science ®Google Scholar
• Liu, L. X., Huang, S., Zhang, Q. Q., Liu, Y., Zhang, D. M., Guo, X. H. and Han, D. W. 2009. Insulin-like growth factor binding protein-7 induces activation and transdifferentiation of hepatic stellate cells in vitro. World J. Gastroenterol. 15:3246–3253.
   PubMedGoogle Scholar
• Mallat, A. and Lotersztajn, S. 2009. Cigarette smoke exposure: A novel cofactor of NAFLD progression? J. Hepatol. 51:430–432.
   PubMedGoogle Scholar
• Mann, J., Oakley, F., Akiboye, F., Elsharkawy, A., Thorne, A. W. and Mann, D. A. 2007. Regulation of myofibroblast transdifferentiation by DNA methylation and MeCP2: Implications for wound healing and fibrogenesis. Cell Death Differ. 14:275–285.
   PubMed Web of Science ®Google Scholar
• Mayhew, T. M., Jenkins, H., Todd, B. and Clifton, V. L. 2008. Maternal asthma and placental morphometry: Effects of severity, treatment and fetal sex. Placenta 29:366–373.
   PubMed Web of Science ®Google Scholar
• Montgomery, S. M. and Ekbom, A. 2002. Smoking during pregnancy and diabetes mellitus in a British longitudinal birth cohort. BMJ 324:26–27.
   PubMed Web of Science ®Google Scholar
• Murphy, V. E., Gibson, P., Talbot, P. I. and Clifton, V. L. 2005. Severe asthma exacerbations during pregnancy. Obstet. Gynecol. 106:1046–1054.
   PubMed Web of Science ®Google Scholar
• Ng SP, Steinetz BG, Lasano SG, and Zelikoff JT. Hormonal changes accompanying cigarette smoke-induced preterm births in a mouse model. Exp Biol Med (Maywood). 2006 Sep;231(8):1403–9.
   PubMedGoogle Scholar
• Niki, T., Rombouts, K., De Bleser, P., De Smet, K., Rogiers, V., Schuppan, D., Yoshida, M., Gabbiani, G. and Geerts, A. 1999. A histone deacetylase inhibitor, trichostatin A, suppresses myofibroblastic differentiation of rat hepatic stellate cells in primary culture. Hepatology 29:858–867.
   PubMed Web of Science ®Google Scholar
• Oken, E., Huh, S. Y., Taveras, E. M., Rich-Edwards, J. W. and Gillman, M. W. 2005. Associations of maternal prenatal smoking with child adiposity and blood pressure. Obes. Res. 13:2021–2028.
   PubMedGoogle Scholar
• Pausová, Z., Paus, T., Sedová, L. and Bérubé, J. 2003. Prenatal exposure to nicotine modifies kidney weight and blood pressure in genetically susceptible rats: A case of gene-environment interaction. Kidney Int. 64:829–835.
   PubMedGoogle Scholar
• Pinzani, M. and Marra, F. 2001. Cytokine receptors and signaling in hepatic stellate cells. Semin. Liver Dis. 21:397–416.
   PubMed Web of Science ®Google Scholar
• Pinzani, M., Milani, S., Herbst, H., DeFranco, R., Grappone, C., Gentilini, A., Caligiuri, A., Pellegrini, G., Ngo, D. V., Romanelli, R. G. and Gentilini, P. 1996. Expression of platelet-derived growth factor and its receptors in normal human liver and during active hepatic fibrogenesis. Am. J. Pathol. 148:785–800.
   PubMed Web of Science ®Google Scholar
• Poynard, T., Bedossa, P. and Opolon, P. 1997. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet 349:825–832.
   PubMed Web of Science ®Google Scholar
• Poynard, T., Lebray, P., Ingiliz, P., Varaut, A., Varsat, B., Ngo, Y., Norha, P., Munteanu, M., Drane, F., Messous, D., Bismut, F. I., Carrau, J. P., Massard, J., Ratziu, V. and Giordanella, J. P. 2010. Prevalence of liver fibrosis and risk factors in a general population using non-invasive biomarkers (FibroTest). BMC Gastroenterol. 10:40.
   PubMed Web of Science ®Google Scholar
• Ramani, K., Yang, H., Kuhlenkamp, J., Tomasi, L., Tsukamoto, H., Mato, J. M. and Lu, S. C. 2010. Changes in the expression of methionine adenosyltransferase genes and S-adenosylmethionine homeostasis during hepatic stellate cell activation. Hepatology 51:986–995.
   PubMed Web of Science ®Google Scholar
• Rinaudo, P. F. and Lamb, J. 2008. Fetal origins of perinatal morbidity and/or adult disease. Semin. Reprod. Med. 26:436–445.
   PubMedGoogle Scholar
• Scott, N. M., Hodyl, N. A., Murphy, V. E., Osei-Kumah, A., Wyper, H., Hodgson, D. M., Smith, R. and Clifton, V. L. 2009. Placental cytokine expression covaries with maternal asthma severity and fetal sex. J. Immunol. 182:1411–1420.
   PubMed Web of Science ®Google Scholar
• Suter, M. A. and Aagaard-Tillery, K. M. 2009. Environmental influences on epigenetic profiles. Semin. Reprod. Med. 27:380–390.
   PubMed Web of Science ®Google Scholar
• Svegliati-Baroni, G., Ridolfi, F., Di Sario, A., Casini, A., Marucci, L., Gaggiotti, G., Orlandoni, P., Macarri, G., Perego, L., Benedetti, A. and Folli, F. 1999. Insulin and insulin-like growth factor-1 stimulate proliferation and type I collagen accumulation by human hepatic stellate cells: Differential effects on signal transduction pathways. Hepatology 29:1743–1751.
   PubMed Web of Science ®Google Scholar
• Syn, W. K., Choi, S. S. and Diehl, A. M. 2009. Apoptosis and cytokines in non-alcoholic steatohepatitis. Clin. Liver Dis. 13:565–580.
   PubMed Web of Science ®Google Scholar
• Williams, S. and Poulton, R. 1999. Twins and maternal smoking: Ordeals for the fetal origins hypothesis? A cohort study. BMJ 318:897–900.
   PubMedGoogle Scholar
• Yasuda, M., Shimizu, I., Shiba, M. and Ito, S. 1999. Suppressive effects of estradiol on dimethylnitrosamine-induced fibrosis of the liver in rats. Hepatology 29:719–727.
   PubMed Web of Science ®Google Scholar
• Zdravkovic, T., Genbacev, O., McMaster, M. T. and Fisher, S. J. 2005. The adverse effects of maternal smoking on the human placenta: A review. Placenta 26 Suppl A:S81–S86.
   Google Scholar
• Zein, C. O., Beatty, K., Post, A. B., Logan, L., Debanne, S. and McCullough, A. J. 2006. Smoking and increased severity of hepatic fibrosis in primary biliary cirrhosis: A cross validated retrospective assessment. Hepatology 44:1564–1571.
   PubMed Web of Science ®Google Scholar