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Hypothesis

Embryonic Resorption and Polycyclic Aromatic Hydrocarbons: Putative Immune-mediated Mechanisms

&
Pages 3-17 | Received 02 May 2009, Accepted 04 Aug 2009, Published online: 14 Jan 2010

REFERENCES

  • Alderete, E., Eskenazi, B. and Sholtm, R. (1995) Effect of cigarette smoking and coffee drinking on time to conception. Epidemiology 6:403–408.
  • Andersson, P., Ridderstad, A., McGuire, J., Pettersson, S., Poellinger, L. and Hanberg, A. (2003) A constitutively active aryl hydrocarbon receptor causes loss of peritoneal B1 cells. Biochem Biophys Res Commun 302:336–341.
  • Archibong, A. E., Inyang, F., Ramesh, A., Greenwood, M., Nayyar, T., Kopsombut, P., Hood, D. B. and Nyanda, A. M. (2002) Alteration of pregnancy related hormones and fetal survival in F-344 rats exposed to inhalation to benzo(a)pyrene. Reproductive Toxicology 16:801–808.
  • Arck, P. C., Rose, M., Hertwig, K., Hagen, E., Hildebrandt, M. and Klapp, B. F. (2001) Stress and immune mediators in miscarriage. Hum Reprod 16:1505–1511.
  • Aschkenazi, S., Straszewski, S., Verwer, K. M., Foellmer, H., Rutherford, T. and Mor, G. (2002) Differential regulation and function of the Fas/Fas ligand system in human trophoblast cells. Biol Reprod 66:1853–1861.
  • Ashkar, A. A., Di Santo, J. P. and Croy, B. A. (2000) Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med 192:259–270.
  • Augood, C., Duckitt, K. and Templeton, A. A. (1998) Smoking and female infertility: A systematic review and meta-analysis. Hum Reprod 13:1532–1539.
  • Baek, K. H. (2004) Aberrant gene expression associated with recurrent pregnancy loss. Mol Hum Reprod 10:291–297.
  • Becher, G. and Bjorseth, A. (1983) Determination of exposure to poly-cyclic aromatic hydrocarbons by analysis of human urine. Cancer Lett 17:301–311.
  • Bobak, M. and Leon, D. A. (1992) Air pollution and infant mortality in the Czech Republic, 1986–88. Lancet 340:1010–1014.
  • Bogovic Crncic, T., Laskarin, G., Juretic, K., Strbo, N., Dupor, J., Srsen, S., Randic, L., Le Bouteiller, P., Tabiasco, J. and Rukavina, D. (2005) Perforin and Fas/FasL cytolytic pathways at the maternal-fetal interface. Am J Reprod Immunol 54:241–248.
  • Booker, C. D. and White, K. L., Jr. (2005) Benzo(a)pyrene-induced anemia and splenomegaly in NZB/WF1 mice. Food Chem Toxicol 43:1423–1431.
  • Bui, Q. Q., Tran, M. B. and West, W. L. (1986) A comparative study of the reproductive effects of methadone and benzo(a)pyrene in the pregnant and pseudopregnant rat. Toxicology 42:195–204.
  • Bulay, O. M. and Wattenberg, L. W. (1971) Carcinogenic effects of polycyclic hydrocarbon carcinogen administration to mice during pregnancy on the progeny. J Natl Cancer Inst 46:397–402.
  • Burchiel, S. W. and Luster, M. I. (2001) Signaling by environmental polycyclic aromatic hydrocarbons in human lymphocytes. Clin Immunol 98:2–10.
  • Carter, A. M. (2006) Animal models of human placentation—a review. Placenta 28(Suppl A):S41–S47.
  • Chaouat, G. (2003) Innately moving away from the Th1/Th2 paradigm in pregnancy. Clin Exp Immunol 131:393–395.
  • Chatenoud, L., Parazzini, F., di Cintio, E., Zanconato, G., Benzi, G., Bortolus, R. and La Vecchia, C. (1998) Paternal and maternal smoking habits before conception and during the first trimester: Relation to spontaneous abortion. Ann Epidemiol 8:520–526.
  • Cheon, H., Woo, Y. S., Lee, J. Y., Kim, H. S., Kim, H. J., Cho, S., Won, N. H. and Sohn, J. (2007) Signaling pathway for 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced TNF-alpha production in differentiated THP-1 human macrophages. Exp Mol Med 39:524–534.
  • Christiansen, O. B., Nybo Andersen, A. M., Bosch, E., Daya, S., Delves, P. J., Hviid, T. V., Kutteh, W. H., Laird, S. M., Li, T. C. and van der Ven, K. (2005) Evidence-based investigations and treatments of recurrent pregnancy loss. Fertil Steril 83:821–839.
  • Cnattingius, S. (2004) The epidemiology of smoking during pregnancy: Smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine Tob Res 6(Suppl 2):S125–140.
  • Cnattingius, S., Lindmark, G. and Meirik, O. (1992) Who continues to smoke while pregnant? Journal of Epidemiology and Community Health 46:218–221.
  • Costenbader, K. H. and Karlson, E. W. (2006) Cigarette smoking and autoimmune disease: What can we learn from epidemiology? Lupus 15:737–745.
  • Cross, J. C. (2005) How to make a placenta: Mechanisms of trophoblast cell differentiation in mice–a review. Placenta 26(Suppl A):S3–9.
  • Cross, J. C., Hemberger, M., Lu, Y., Nozaki, T., Whiteley, K., Masutani, M. and Adamson, S. L. (2002) Trophoblast functions, angiogenesis and remodeling of the maternal vasculature in the placenta. Mol Cell Endocrinol 187:207–212.
  • Croy, B. A., Chantakru, S., Esadeg, S., Ashkar, A. A. and Wei, Q. (2002) Decidual natural killer cells: Key regulators of placental development (a review). Journal of Reproductive Immunology 57:151–168.
  • Croy, B. A., He, H., Esadeg, S., Wei, Q., McCartney, D., Zhang, J., Borzychowski, A., Ashkar, A. A., Black, G. P., Evans, S. S., et al. (2003a) Uterine natural killer cells: Insights into their cellular and molecular biology from mouse modelling. Reproduction 126:149–160.
  • Croy, B. A., Esadeg, S., Chantakru, S., van den Heuvel, M., Paffaro, V. A., He, H., Black, G. P., Ashkar, A. A., Kiso, Y. and Zhang, J. (2003b) Update on pathways regulating the activation of uterine Natural Killer cells, their interactions with decidual spiral arteries and homing of their precursors to the uterus. Journal of Reproductive Immunology 59:175–191.
  • Croy, B. A. and Kiso, Y (1993) Granulated metrial gland cells: A natural killer cell subset of the pregnant murine uterus. Microsc Res Tech 25:189–200.
  • Croy, B. A., McBey, B. A., Villeneuve, L. A., Kusakabe, K., Kiso, Y and van den Heuvel, M. (1997) Characterization of the cells that migrate from metrial glands of the pregnant mouse uterus during explant culture. J Reprod Immunol 32:241–263.
  • Croy, B. A., Rossant, J. and Clark, D. A. (1982) Histological and immunological studies of post implantation death of Mus caroli embryos in the Mus musculus uterus. J Reprod Immunol 4:277–293.
  • Dang, Y., Beckers, J., Wang, C. R. and Heyborne, K. D. (2000) Natural killer 1.1 ( + ) alpha beta T cells in the periimplantation uterus. Immunology 101:484–491.
  • Das, S. N., Paul, B. N., Saxena, A. K. and Ray, P. K. (1990) Effect of in utero exposure to hexachlorocyclohexane on the developing immune system of mice. Immunopharmacol Immunotoxicol 12:293–310.
  • de Fougerolles, A. R. and Baines, M. G. (1987) Modulation of the natural killer cell activity in pregnant mice alters the spontaneous abortion rate. J Reprod Immunol 11:147–153.
  • Dean, J. H., Ward, E. C., Murray, M. J., Lauer, L. D., House, R. V., Stillman, W., Hamilton, T. A. and Adams, D. O. (1986) Immunosuppression following 7,12-dimethylbenz[a]anthracene exposure in B6C3F1 mice—II. Altered cell-mediated immunity and tumor resistance. Int J Immunopharmacol 8:189–198.
  • Delgado, S. R., McBey, B. A., Yamashiro, S., Fujita, J., Kiso, Y. and Croy, B. A. (1996) Accounting for the peripartum loss of granulated metrial gland cells, a natural killer cell population, from the pregnant mouse uterus. J Leukoc Biol 59:262–269.
  • Detmar, J., Rabaglino, T., Taniuchi, Y., Oh, J., Acton, B. M., Benito, A., Nunez, G. and Jurisicova, A. (2006) Embryonic loss due to exposure to polycyclic aromatic hydrocarbons is mediated by Bax. Apoptosis 11:1413–1425.
  • Detmar, J., Rennie, M. Y., Whiteley, K. J., Qu, D., Taniuchi, Y., Shang, X., Casper, R. F., Adamson, S. L., Sled, J. G. and Jurisicova, A. (2008) Fetal growth restriction triggered by polycyclic aromatic hydrocarbons is associated with altered placental vasculature and AhR-dependent changes in cell death. American journal of physiology. Endocrinology and metabolism 295:E519–530.
  • Donaghay, M. and Lessey, B. A. (2007) Uterine receptivity: Alterations associated with benign gynecological disease. Semin Reprod Med 25:461–475.
  • Egawa, M., Yasuda, K., Nakajima, T., Okada, H., Yoshimura, T., Yuri, T., Yasuhara, M., Nakamoto, T., Nagata, F. and Kanzaki, H. (2003) Smoking enhances oxytocin-induced rhythmic myometrial contraction. Biol Reprod 68:2274–2280.
  • Esposito, E. R., Horn, K. H., Greene, R. M. and Pisano, M. M. (2008) An animal model of cigarette smoke-induced in utero growth retardation. Toxicology 246:193–202.
  • Farkas, S., Hussein, J., Ariano, R. E., Sitar, D. S. and Hasan, S. U. (2006) Prenatal cigarette smoke exposure: Pregnancy outcome and gesta-tional changes in plasma nicotine concentration, hematocrit, and carboxyhemoglobin in a newly standardized rat model. Toxicol Appl Pharmacol 214:118–125.
  • Fernandez-Salguero, P., Pineau, T., Hilbert, D. M., McPhail, T., Lee, S. S., Kimura, S., Nebert, D. W., Rudikoff, S., Ward, J. M. and Gonzalez, F. J. (1995) Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268:722–726.
  • Fernandez-Salguero, P. M., Ward, J. M., Sundberg, J. P. and Gonzalez, F. J. (1997) Lesions of aryl-hydrocarbon receptor-deficient mice. Vet Pathol 34:605–614.
  • Fingerhut, L. A., Kleinman, J. C. and Kendrick, J. S. (1990) Smoking before, during, and after pregnancy. American Journal of Public Health 80:541–544.
  • Fischer, B. (2000) Receptor-mediated effects of chlorinated hydrocarbons. Andrologia 32:279–283.
  • Frericks, M., Meissner, M. and Esser, C. (2007) Microarray analysis of the AHR system: Tissue-specific flexibility in signal and target genes. Toxicol Appl Pharmacol 220:320–332.
  • Gendron, R. L. and Baines, M. G. (1988) Infiltrating decidual natural killer cells are associated with spontaneous abortion in mice. Cell Immunol 113:261–267.
  • George, L., Granath, F., Johansson, A. L., Anneren, G. and Cnattingius, S. (2006) Environmental tobacco smoke and risk of spontaneous abortion. Epidemiology 17:500–505.
  • Georgiades, P., Ferguson-Smith, A. C. and Burton, G. J. (2002) Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23:3–19.
  • Germolec, D. R., Henry, E. C., Maronpot, R., Foley, J. F., Adams, N. H., Gasiewicz, T. A. and Luster, M. I. (1996) Induction of CYP1A1 and ALDH-3 in ymphoid tissues from Fisher 344 rats exposed to 2,3,7,8-tetrachlorodibenzodioxin (TCDD). Toxicol Appl Pharmacol 137:57–66.
  • Gilliland, F. D., Li, Y F. and Peters, J. M. (2001) Effects of maternal smoking during pregnancy and environmental tobacco smoke on asthma and wheezing in children. Am J Respir Crit Care Med 163:429–436.
  • Girardi, G. (2008) Guilty as charged: All available evidence implicates complement's role in fetal demise. Am J Reprod Immunol 59:183–192.
  • Girardi, G., Berman, J., Redecha, P., Spruce, L., Thurman, J. M., Kraus, D., Hollmann, T. J., Casali, P., Caroll, M. C., Wetsel, R. A., et al. (2003) Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J Clin Invest 112:1644–1654.
  • Gladen, B. C., Zadorozhnaja, T. D., Chislovska, N., Hryhorczuk, D. O., Kennicutt, M. C., 2nd and Little, R. E. (2000) Polycyclic aromatic hydrocarbons in placenta. Hum Exp Toxicol 19:597–603.
  • Grimmer, G., Stober, W., Jacob, J., Mohr, U., Schoene, K., Brune, H. and Misfeld, J. (1983) Inventory and biological impact of polycyclic carcinogens in the environment. Exp Pathol 24:3–13.
  • Gruslin, A., Qiu, Q. and Tsang, B. K. (2001)X-linked inhibitor of apoptosis protein expression and the regulation of apoptosis during human placental development. Biol Reprod 64:1264–1272.
  • Guimond, M. J., Wang, B. and Croy, B. A. (1998) Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. J Exp Med 187:217–223.
  • Hanna, J., Goldman-Wohl, D., Hamani, Y., Avraham, I., Greenfield, C., Natanson-Yaron, S., Prus, D., Cohen-Daniel, L., Arnon, T. I., Manaster, I., et al. (2006) Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 12:1065–1074.
  • Hansen, C., Sorensen, L. D., Asmussen, I. and Autrup, H. (1992) Trans-placental exposure to tobacco smoke in human-adduct formation in placenta and umbilical cord blood vessels. Teratog Carcinog Mutagen 12:51–60.
  • Hansen, J. M., Reynolds, P. R., Booth, G. M., Schaalje, G. and Seegmiller, R. E. (2000) Developmental toxicity of carbon black oil in mice. Teratology 62:227–232.
  • Hardy, K., Spanos, S., Becker, D., Iannelli, P., Winston, R. M. and Stark, J. (2001) From cell death to embryo arrest: Mathematical models of human preimplantation embryo development. Proc Natl Acad Sci USA 98:1655–1660.
  • Harlap, S. and Shiono, P. H. (1980) Alcohol, smoking, and incidence of spontaneous abortions in the first and second trimester. Lancet 2:173–176.
  • Heaman, M. I. and Chalmers, K. (2005) Prevalence and correlates of smoking during pregnancy: A comparison of aboriginal and non-aboriginal women in manitoba. Birth 32:299–305.
  • Higgins, S. (2002) Smoking in pregnancy. Current Opinion in Obstetrics and Gynecology 14:145–151.
  • Hill, J. A., Polgar, K. and Anderson, D. J. (1995)T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. Jama 273:1933–1936.
  • Himmelberger, D. U., Brown, B. W., Jr. and Cohen, E. N. (1978) Cigarette smoking during pregnancy and the occurrence of spontaneous abortion and congenital abnormality. Am J Epidemiol 108:470–479.
  • Hoffmann, D. and Hoffmann, I. (1997) The changing cigarette, 1950–1995. J Toxicol Environ Health 50:307–364.
  • Holladay, S. D. and Smialowicz, R. J. (2000) Development of the murine and human immune system: Differential effects of immunotoxicants depend on time of exposure. Environ Health Perspect 108(Suppl 3): 463–473.
  • Howard, J. W. and Fazio, T. (1980) Analytical methodology and reported findings of polycyclic aromatic hydrocarbons in foods. J Assoc Off Anal Chem 63:1077–1104.
  • Howe, G., Westhoff, C., Vessey, M. and Yeates, D. (1985) Effects of age, cigarette smoking and other factors on fertility: Findings in a large prospective study. British Medical Journal 290:1697–1700.
  • Huang, J., Okuka, M., McLean, M., Keefe, D. L. and Liu, L. (2008) Effects of cigarette smoke on fertilization and embryo development in vivo. http://www.fertstert.org/article/S0015–0282(08)03563–2/pdf 28 February 2009.
  • Hunt, J. S. (2006) Stranger in a strange land. Immunol Rev 213:36–47.
  • Hunt, J. S., Chu, W. and Miller, L. (1998) Nonspecific immunity in the uterus and placenta. Trophoblast Research 12:125–134.
  • Hunt, J. S., Vassmer, D., Ferguson, T. A. and Miller, L. (1997) Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J Immunol 158:4122–4128.
  • 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.
  • Jerzak, M. and Bischof, P. (2002) Apoptosis in the first trimester human placenta: The role in maintaining immune privilege at the maternal-foetal interface and in the trophoblast remodelling. Eur J Obstet Gynecol Reprod Biol 100:138–142.
  • Joesoef, M. R., Beral, V., Aral, S. O., Rolfs, R. T. and Cramer, D. W. (1993) Fertility and use of cigarettes, alcohol, marijuana and cocaine. Annals of Epidemiology 3:592–594.
  • Kadkhoda, K., Pourpak, Z., Akbar Pourfathallah, A. and Kazemnejad, A. (2004) The ex vivo study of synergistic effects of polycyclic aromatic hydrocarbon, benzo(a)pyrene with ovalbumin on systemic immune responses by oral route. Toxicology 199:261–265.
  • Kahn, R. S., Certain, L. and Whitaker, R. C. (2002) A reexamination of smoking before, during, and after pregnancy. Am J Public Health 92:1801–1808.
  • Karakaya, A., Ates, I. and Yucesoy, B. (2004) Effects of occupational polycyclic aromatic hydrocarbon exposure on T-lymphocyte functions and natural killer cell activity in asphalt and coke oven workers. Hum ExpToxicol 23:317–322.
  • Khan, H. M., Khan, M. Y. and Minhas, L. A. (2008) Effect of passive tobacco smoking on fertility of female mice. J Coll Physicians Surg Pak 18:708–712.
  • Khorram, O., Han, G. and Magee, T. (2008) Cigarette smoke inhibits endometrial epithelial cell proliferation through a nitric oxide-mediated pathway. http://www.fertstert.org/article/S0015–0282(08)04101 -0/pdf 6 March 2009.
  • Kim, D. W., Gazourian, L., Quadri, S. A., Romieu-Mourez, R., Sherr, D. H. and Sonenshein, G. E. (2000) The RelA NF-kappaB subunit and the aryl hydrocarbon receptor (AhR) cooperate to transactivate the c-myc promoter in mammary cells. Oncogene 19:5498–5506.
  • King, A., Jokhi, P. P., Burrows, T. D., Gardner, L., Sharkey, A. M. and Loke, Y. W. (1996) Functions of human decidual NK cells. Am J Reprod Immunol 35:258–260.
  • King, A. and Loke, Y W. (1990) Human trophoblast and JEG chorio-carcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell Immunol 129:435–448.
  • Kitamura, M. and Kasai, A. (2007) Cigarette smoke as a trigger for the dioxin receptor-mediated signaling pathway. Cancer Lett 252:184–194.
  • Klareskog, L., Padyukov, L. and Alfredsson, L. (2007) Smoking as a trigger for inflammatory rheumatic diseases. Curr Opin Rheumatol 19:49–54.
  • Kline, J., Levin, B., Kinney, A., Stein, Z., Susser, M. and Warburton, D. (1995) Cigarette smoking and spontaneous abortion of known karyotype. Precise data but uncertain inferences. Am J Epidemiol 141:417–427.
  • Kline, J., Stein, Z. A., Suser, M. and Warburton, D. (1977) Smoking: A risk factor for spontaneous abortion. New England Journal of Medicine 297:793–796.
  • Kusakabe, K., Okada, T., Sasaki, F. and Kiso, Y (1999) Cell death of uterine natural killer cells in murine placenta during placentation and preterm periods. J Vet Med Sci 61:1093–1100.
  • Lecureur, V., Ferrec, E. L., N'Diaye, M., Vee, M. L., Gardyn, C., Gilot, D. and Fardel, O. (2005) ERK-dependent induction of TNFalpha expression by the environmental contaminant benzo(a)pyrene in primary human macrophages. FEBS Lett 579:1904–1910.
  • Lederman, S. A., Rauh, V., Weiss, L., Stein, J. L., Hoepner, L. A., Becker, M. and Perera, F. P. (2004) The effects of the World Trade Center event on birth outcomes among term deliveries at three lower Manhattan hospitals. Environ Health Perspect 112:1772–1778.
  • Lee, J., Choi, B. C., Cho, C., Hill, J. A., Baek, K. H. and Kim, J. W. (2005) Trophoblast apoptosis is increased in women with evidence of TH1 immunity. Fertil Steril 83:1047–1049.
  • Liang, S., Zhang, J., Wei, H., Sun, R. and Tian, Z. (2005) Differential roles of constitutively activated ERK1/2 and NF-kappa B in cytotoxicity and proliferation by human NK cell lines. Int Immunopharmacol 5:839–848.
  • Lin, H., Mosmann, T. R., Guilbert, L., Tuntipopipat, S. and Wegmann, T. G. (1993) Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 151:4562–4573.
  • Lintsen, A. M., Pasker-de Jong, P. C., de Boer, E. J., Burger, C. W., Jansen, C. A., Braat, D. D. and van Leeuwen, F. E. (2005) Effects of subfertility cause, smoking and body weight on the success rate of IVF. Hum Reprod 20:1867–1875.
  • Lioy, P. J., Weisel, C. P., Millette, J. R., S. Eisenreich, S., Vallero, D., Offenberg, J., Buckley, B., Turpin, B., Zhong, M., Cohen, M. D., . (2002) Characterization of the dust/smoke aerosol that settled east of the World Trade Center (WTC) in lower Manhattan after the collapse of the WTC 11 September 2001. Environ Health Perspect 110:703–714.
  • Luppi, P., Haluszczak, C., Betters, D., Richard, C. A., Trucco, M. and DeLoia, J. A. (2002) Monocytes are progressively activated in the circulation of pregnant women. J Leukoc Biol 72:874–884.
  • Mackenzie, K. M. and Angevine, D. M. (1981) Infertility in mice exposed in utero to benzo(a)-pyrene. Biology of Reproduction 24:183–191.
  • Magnusson, C. G. (1986) Maternal smoking influences cord serum IgE and IgD levels and increases the risk for subsequent infant allergy. J Allergy Clin Immunol 78:898–904.
  • Marx, L., Arck, P., Kieslich, C., Mitterlechner, S., Kapp, M. and Dietl, J. (1999) Decidual mast cells might be involved in the onset of human first-trimester abortion. Am J Reprod Immunol 41:34–40.
  • Marzi, M., Vigano, A., Trabattoni, D., Villa, M. L., Salvaggio, A., Clerici, E. and Clerici, M. (1996) Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin Exp Immunol 106:127–133.
  • Matiasovic, J., Leva, L., Maskova, J., Kummer, V and Faldyna, M. (2008) Effects of postnatal exposure to benzo[a]pyrene on the immunity of immature rats. Veterinarni Medicina 53:93–100.
  • Matsubayashi, H., Shida, M., Kondo, A., Suzuki, T., Sugi, T., Izumi, S., Hosaka, T. and Makino, T. (2005) Preconception peripheral natural killer cell activity as a predictor of pregnancy outcome in patients with unexplained infertility. Am J Reprod Immunol 53:126–131.
  • Meeker, J. D., Missmer, S. A., Vitonis, A. F., Cramer, D. W. and Hauser, R. (2007) Risk of spontaneous abortion in women with childhood exposure to parental cigarette smoke. Am J Epidemiol 166:571–575.
  • Mlynarcikova, A., Fickova, M. and Scsukova, S. (2005) Ovarian intra-follicular processes as a target for cigarette smoke components and selected environmental reproductive disruptors. Endocr Regul 39:21–32.
  • Moffett-King, A. (2002) Natural killer cells and pregnancy. Nat Rev Immunol 2:656–663.
  • Moffett, A. and Loke, C. (2006) Immunology of placentation in eutherian mammals. Nat Rev Immunol 6:584–594.
  • Molina, V and Shoenfeld, Y (2005) Infection, vaccines and other environmental triggers of autoimmunity. Autoimmunity 38:235–245.
  • Motz, G. T., Eppert, B. L., Sun, G., Wesselkamper, S. C., Linke, M. J., Deka, R. and Borchers, M. T. (2008) Persistence of lung CD8 Tcell oligoclonal expansions upon smoking cessation in a mouse model of cigarette smoke-induced emphysema. J Immunol 181:8036–8043.
  • Murphy, S. P., Fast, L. D., Hanna, N. N. and Sharma, S. (2005) Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J Immunol 175:4084–4090.
  • Nakamoto, T., Yasuda, K., Yasuhara, M., Nakajima, T., Mizokami, T., Okada, H. and Kanzaki, H. (2006) Cigarette smoke extract enhances oxytocin-induced rhythmic contractions of rat and human preterm myometrium. Reproduction 132:343–353.
  • Nakashima, A., Shiozaki, A., Myojo, S., Ito, M., Tatematsu, M., Sakai, M., Takamori, Y., Ogawa, K., Nagata, K. and Saito, S. (2008) Granulysin produced by uterine natural killer cells induces apoptosis of extravillous trophoblasts in spontaneous abortion. Am J Pathol 173:653–664.
  • Neal, M. S., Hughes, E. G., Holloway, A. C. and Foster, W. G. (2005) Side-stream smoking is equally as damaging as mainstream smoking on IVF outcomes. Hum Reprod 20:2531–2535.
  • Ness, R. B., Grisso, J. A., Hirschinger, N., Markovic, N., Shaw, L. M., Day, N. L. and Kline, J. (1999) Cocaine and tobacco use and the risk of spontaneous abortion. New England Journal of Medicine 340:333–339.
  • Ng, S. P. and Zelikoff, J. T. (2008) The effects of prenatal exposure of mice to cigarette smoke on offspring immune parameters. J Toxicol Environ Health A 71:445–453.
  • Nishikawa, K., Saito, S., Morii, T., Hamada, K., Ako, H., Narita, N., Ichijo, M., Kurahayashi, M. and Sugamura, K. (1991) Accumulation of CD16-CD56+ natural killer cells with high affinity interleukin 2 receptors in human early pregnancy decidua. Int Immunol 3:743–750.
  • Noakes, P. S., Holt, P. G. and Prescott, S. L. (2003) Maternal smoking in pregnancy alters neonatal cytokine responses. Allergy 58:1053–1058.
  • Nohara, K., Pan, X., Tsukumo, S., Hida, A., Ito, T., Nagai, H., Inouye, K., Motohashi, H., Yamamoto, M., Fujii-Kuriyama, Y. and Tohyama, C. (2005) Constitutively active aryl hydrocarbon receptor expressed specifically in T-lineage cells causes thymus involution and suppresses the immunization-induced increase in splenocytes. J Immunol 174:2770–2777.
  • Offenberg, J. H., Eisenreich, S. J., Chen, L. C., Cohen, M. D., Chee, G., Prophete, C., Weisel, C. and Lioy, P. J. (2003) Persistent organic pollutants in the dusts that settled across lower Manhattan after September 11, 2001. Environ Sci Technol 37:502–508.
  • Olivares, E. G., Munoz, R., Tejerizo, G., Montes, M. J., Gomez-Molina, F. and Abadia-Molina, A. C. (2002) Decidual lymphocytes of human spontaneous abortions induce apoptosis but not necrosis in JEG-3 extravillous trophoblast cells. Biol Reprod 67:1211–1217.
  • Osorio, Y., Bonilla, D. L., Peniche, A. G., Melby, P. C. and Travi, B. L. (2008) Pregnancy enhances the innate immune response in experi mental cutaneous leishmaniasis through hormone-modulated nitric oxide production. J Leukoc Biol 83:1413–1422.
  • Parham, P. (2004) NK cells and trophoblasts: Partners in pregnancy. J Exp Med 200:951–955.
  • Parr, E. L., Parr, M. B., Zheng, L. M. and Young, J. D. (1991) Mouse granulated metrial gland cells originate by local activation of uterine natural killer lymphocytes. Biol Reprod 44:834–841.
  • Peel, S. (1989) Granulated metrial gland cells. Adv Anat Embryol Cell Biol 115:1–112.
  • Pejcic-Karapetrovic, B., Gurnani, K., Russell, M. S., Finlay, B. B., Sad, S. and Krishnan, L. (2007) Pregnancy impairs the innate immune resistance to Salmonella typhimurium leading to rapid fatal infection. J Immunol 179:6088–6096.
  • Perera, F. P., Tang, D., Rauh, V., Lester, K., Tsai, W. Y., Tu, Y H., Weiss, L., Hoepner, L., King, J., Del Priore, G. and Lederman, S. A. (2005a) Relationships among polycyclic aromatic hydrocarbon-DNA adducts, proximity to the World Trade Center, and effects on fetal growth. Environ Health Perspect 113:1062–1067.
  • Perera, F., Tang, D., Whyatt, R., Lederman, S. A. and Jedrychowski, W. (2005b) DNA damage from polycyclic aromatic hydrocarbons measured by benzo[a]pyrene-DNA adducts in mothers and newborns from Northern Manhattan, the World Trade Center Area, Poland, and China. Cancer Epidemiol Biomarkers Prev 14:709–714.
  • Piccinni, M. P. and Romagnani, S. (1996) Regulation of fetal allograft survival by a hormone-controlled Th1- and Th2-type cytokines. Immunol Res 15:141–150.
  • Pocar, P., Fischer, B., Klonisch, T. and Hombach-Klonisch, S. (2005) Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Reproduction 129:379–389.
  • Qiu, Q., Yang, M., Tsang, B. K. and Gruslin, A. (2005) Fas ligand expression by maternal decidual cells is negatively correlated with the abundance of leukocytes present at the maternal-fetal interface. J Reprod Immunol 65:121–132.
  • Quenby, S., Nik, H., Innes, B., Lash, G., Turner, M., Drury, J. and Bulmer, J. (2009) Uterine natural killer cells and angiogenesis in recurrent reproductive failure. Hum Reprod 24:45–54.
  • Quintana, F. J., Basso, A. S., Iglesias, A. H., Korn, T., Farez, M. F., Bettelli, E., Caccamo, M., Oukka, M. and Weiner, H. L. (2008) Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453:65–71.
  • Raine-Fenning, N. J., Campbell, B. K., Kendall, N. R., Clewes, J. S. and Johnson, I. R. (2004) Quantifying the changes in endometrial vascularity throughout the normal menstrual cycle with three-dimensional power Doppler angiography. Hum Reprod 19:330–338.
  • Redman, C. W. and Sargent, I. L. (2003) Pre-eclampsia, the placenta and the maternal systemic inflammatory response—A review. Placenta 24(Suppl A):S21–27.
  • Richani, K., Soto, E., Romero, R., Espinoza, J., Chaiworapongsa, T., Nien, J. K., Edwin, S., Kim, Y. M., Hong, J. S. and Mazor, M. (2005) Normal pregnancy is characterized by systemic activation of the complement system. J Matern Fetal Neonatal Med 17:239–245.
  • Rogerson, S. J., Pollina, E., Getachew, A., Tadesse, E., Lema, V. M. and Molyneux, M. E. (2003) Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. Am J Trop Med Hyg 68:115–119.
  • Rushton, L. (2007) Occupational causes of chronic obstructive pulmonary disease. Rev Environ Health 22:195–212.
  • Sacks, G. P., Clover, L. M., Bainbridge, D. R., Redman, C. W. and Sargent, I. L. (2001) Flow cytometric measurement of intracellular Th1 and Th2 cytokine production by human villous and extravillous cytotrophoblast. Placenta 22:550–559.
  • Sargent, I. L., Borzychowski, A. M. and Redman, C. W. (2006) NK cells and human pregnancy–an inflammatory view. Trends Immunol 27:399–404.
  • Schmidt, J. V., Su, G. H., Reddy, J. K., Simon, M. C. and Bradfield, C. A. (1996) Characterization of a murine Ahr null allele: Involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci U S A 93:6731–6736.
  • Seavey, M. M. and Mosmann, T. R. (2008) Immunoregulation of fetal and anti-paternal immune responses. Immunol Res 40:97–113.
  • Sharara, F. I., Seifer, D. B. and Flaws, J. A. (1998) Environmental toxicants and female reproduction. Fertil Steril 70:613–622.
  • Sharkey, A. M., Gardner, L., Hiby, S., Farrell, L., Apps, R., Masters, L., Goodridge, J., Lathbury, L., Stewart, C. A., Verma, S. and Moffett, A. (2008) Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age. J Immunol 181:39–46.
  • Shiverick, K. T. and Salafia, C. (1999) Cigarette smoking and pregnancy I: Ovarian, uterine and placental effects. Placenta 20:265–272.
  • Soares, S. R. and Melo, M. A. (2008) Cigarette smoking and reproductive function. Curr Opin Obstet Gynecol 20:281–291.
  • Soares, S. R., Simon, C., Remohi, J. and Pellicer, A. (2007) Cigarette smoking affects uterine receptiveness. Hum Reprod 22:543–547.
  • Soghomonians, A., Thirkill, T. L., Mariano, N. F., Barakat, A. I. and Douglas, G. C. (2004) Effect of aqueous tobacco smoke extract and shear stress on PECAM-1 expression and cell motility in human uterine endothelial cells. Toxicol Sci 81:408–418.
  • Sopori, M. (2002) Effects of cigarette smoke on the immune system. Nat Rev Immunol 2:372–377.
  • Sram, R. (1999) Impact of air pollution on reproductive health. Environ Health Perspect 107:A542–543.
  • Stevens, E. A. and Bradfield, C. A. (2008) Immunology: Tcells hang in the balance. Nature 453:46–47.
  • Tauchi, M., Hida, A., Negishi, T., Katsuoka, F., Noda, S., Mimura, J., Hosoya, T., Yanaka, A., Aburatani, H., Fujii-Kuriyama, Y., et al. (2005) Constitutive expression of aryl hydrocarbon receptor in keratinocytes causes inflammatory skin lesions. Mol Cell Biol 25:9360–9368.
  • Thirkill, T. L., Vedagiri, H. and Douglas, G. C. (2006) Macaque trophoblast migration toward RANTES is inhibited by cigarette smoke-conditioned medium. Toxicol Sci 91:557–567.
  • Tian, Y., Ke, S., Denison, M. S., Rabson, A. B. and Gallo, M. A. (1999) Ah receptor and NF-kappaB interactions, a potential mechanism for dioxin toxicity. J Biol Chem 274:510–515.
  • Veldhoen, M., Hirota, K., Christensen, J., O'Garra, A. and Stockinger, B. (2009) Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 Tcells. J Exp Med 206:43–49.
  • Veldhoen, M., Hirota, K., Westendorf, A. M., Buer, J., Dumoutier, L., Renauld, J. C. and Stockinger, B. (2008) The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453:106–109.
  • Venners, S. A., Wang, X., Chen, C., Wang, L., Chen, D., Guang, W., Huang, A., Ryan, L., O'Connor, J., Lasley, B., et al. (2004) Paternal smoking and pregnancy loss: A prospective study using a biomarker of pregnancy. Am J Epidemiol 159:993–1001.
  • Ventura, S. J., Hamilton, B. E., Mathews, T. J. and Chandra, A. (2003) Trends and variations in smoking during pregnancy and low birth weight: Evidence from the birth certificate, 1990–2000. Pediatrics 111:1176–1180.
  • Vestergaard, P., Rejnmark, L., Weeke, J., Hoeck, H. C., Nielsen, H. K., Rungby, J., Laurberg, P. and Mosekilde, L. (2002) Smoking as a risk factor for Graves’ disease, toxic nodular goiter, and autoimmune hypothyroidism. Thyroid 12:69–75.
  • von Rango, U. (2008) Fetal tolerance in human pregnancy—A crucial balance between acceptance and limitation of trophoblast invasion. Immunol Lett 115:21–32.
  • Wang, X., Ding, H., Ryan, L. and Xu, X. (1997) Association between air pollution and low birth weight: A community-based study. Environ Health Perspect 105:514–520.
  • Ward, E. C., Murray, M. J., Lauer, L. D., House, R. V. and Dean, J. H. (1986) Persistent suppression of humoral and cell-mediated immunity in mice following exposure to the polycyclic aromatic hydrocarbon 7,12-dimethylbenz[a]anthracene. Int J Immunopharmacol 8:13–22.
  • Ward, E. C., Murray, M. J., Lauer, L. D., House, R. V., Irons, R. and Dean, J. H. (1984) Immunosuppression following 7,12-dimethylbenz[a]anthracene exposure in B6C3F1 mice. I. Effects on humoral immunity and host resistance. Toxicol Appl Pharmacol 75:299–308.
  • Warren, J. E. and Silver, R. M. (2008) Genetics of pregnancy loss. Clin Obstet Gynecol 51:84–95.
  • Waylen, A. L., Metwally, M., Jones, G. L., Wilkinson, A. J. and Ledger, W. L. (2009) Effects of cigarette smoking upon clinical outcomes of assisted reproduction: A meta-analysis. Hum Reprod Update 15:31–44.
  • Wegmann, T. G., Lin, H., Guilbert, L. and Mosmann, T. R. (1993) Bidirectional cytokine interactions in the maternal-fetal relationship: Is successful pregnancy a TH2 phenomenon? Immunol Today 14:353–356.
  • Whyatt, R. M., Jedrychowski, W., Hemminki, K., Santella, R. M., Tsai, W. Y., Yang, K. and Perera, F. P. (2001) Biomarkers of polycyclic aromatic hydrocarbon-DNA damage and cigarette smoke exposures in paired maternal and newborn blood samples as a measure of differential susceptibility. Cancer Epidemiol Biomarkers Prev 10:581–588.
  • Widayati, D. T., Ohmori, Y. and Fukuta, K. (2004) Distribution patterns of immunocompetent cells in the pregnant mouse uteri carrying allogeneic mouse and xenogeneic vole embryos. J Anat 205:45–55.
  • Wilcox, A. J., Weinberg, C. R., O'Connor, J. F., Baird, , Schlatterer, J. P., Canfield, R. E., Armstrong, E. G. and Nisula, B. C. (1988) Incidence of early loss of pregnancy. N Engl J Med 319:189–194.
  • Witschi, H., Joad, J. P. and Pinkerton, K. E. (1997) The toxicology of environmental tobacco smoke. Annual Reviews in Pharmacology and Toxicology 37:29–52.
  • Woodruff, T. J., Grillo, J. and Schoendorf, K. C. (1997) The relationship between selected causes of postneonatal infant mortality and particulate air pollution in the United States. Environ Health Perspect 105:608–612.
  • Wordinger, R. J., Jackson, F. L. and Morrill, A. (1986) Implantation, deciduoma formation and live births in mast cell-deficient mice (W/Wv). J Reprod Fertil 77:471–476.
  • Wu, X., Wei, H., Zhang, J. and Tian, Z. (2006) Increased uterine NK- derived IFN-gamma and TNF-alpha in C57BL/6J mice during early gestation. Cell Mol Immunol 3:131–137.
  • Yusuf, N., Timares, L., Seibert, M. D., Xu, H. and Elmets, C. A. (2007) Acquired and innate immunity to polyaromatic hydrocarbons. Toxicol Appl Pharmacol 224:308–312.
  • Zenclussen, A. C. (2005) CD4( + )CD25+ T regulatory cells in murine pregnancy. J Reprod Immunol 65:101–110.
  • Zenzes, M. T., Wang, P. and Casper, R. F. (1995) Cigarette smoking may affect meiotic maturation of human oocytes. Hum Reprod 10:3213–3217.
  • Zhang, J. and Tian, Z. (2007) UNK cells: Their role in tissue re-modelling and preeclampsia. Semin Immunopathol 29:123–133.
  • Zinaman, M. J., Clegg, E. D., Brown, C. C., O'Connor, J. and Selevan, S. G. (1996) Estimates of human fertility and pregnancy loss. Fertil Steril 65:503–509.

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