Developmental dioxin exposure of either parent is associated with an increased risk of preterm birth in adult mice

Reproductive Toxicology

Volumn 31, Issue 3, 2011, Pages 351-358

  Ding, Tianbing ^a   McConaha, Melinda ^a   Boyd, Kelli L ^a   Osteen, Kevin G ^a   Bruner Tran, Kaylon L ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Decidua; Inflammation; Mice; Placenta; Preterm birth; Progesterone receptor; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; DIOXIN; PROGESTERONE RECEPTOR; PROTEIN P105; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR 4;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECIDUA; DOWN REGULATION; EARLY LIFE STRESS; FEMALE; FEMALE FERTILITY; MALE; MOUSE; NONHUMAN; ORGAN WEIGHT; PREGNANCY OUTCOME; PREMATURE LABOR; PRENATAL EXPOSURE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RISK FACTOR; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED C57BL; PATERNAL EXPOSURE; PLACENTA; PLACENTA DISEASES; PREGNANCY; PREMATURE BIRTH; PRENATAL EXPOSURE DELAYED EFFECTS; RECEPTORS, PROGESTERONE; RNA, MESSENGER; TERATOGENS; TETRACHLORODIBENZODIOXIN;

MAMMALIA; MUS;

EID: 79953759048     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2010.11.003     Document Type: Article

References (61)

1. Henson M.C. Pregnancy maintenance and the regulation of placental progesterone biosynthesis in the baboon. Hum Reprod Update 1998, 4:389-405.
2. Kramer M.S., Demissie K., Yang H., Platt R.W., Sauve R., Liston R. The contribution of mild and moderate preterm birth to infant mortality. Fetal and Infant Health Study Group of the Canadian Perinatal Surveillance System. JAMA 2000, 284:843-849.
3. Schindler A.E. Role of progestogens for the prevention of premature birth. J Steroid Biochem Mol Biol 2005, 97:435-438.
4. March of Dimes website. Available from:, [cited: August 22, 2010]. http://www.marchofdimes.com/.
5. Holzman C., Eyster J., Kleyn M., Messer L.C., Kaufman J.S., Laraia B.A., et al. Maternal weathering and risk of preterm delivery. Am J Public Health 2009, 99:1864-1871.
6. Kitamura M., Kasai A. Cigarette smoke as a trigger for the dioxin receptor-mediated signaling pathway. Cancer Lett 2007, 252:184-194.
7. Heindel J.J. Role of exposure to environmental chemicals in the developmental basis of reproductive disease and dysfunction. Semin Reprod Med 2006, 24:168-177.
8. Mattison D.R. Environmental exposures and development. Curr Opin Pediatr 2010, 22:208-218.
9. Bruner-Tran K.L., Osteen K.G. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod Toxicol 2011, 31:344-350.
10. Nayyar T., Bruner-Tran K.L., Piestrzeniewicz-Ulanska D., Osteen K.G. Developmental exposure of mice to TCDD elicits a similar uterine phenotype in adult animals as observed in women with endometriosis. Reprod Toxicol 2007, 23:326-336.
11. Bruner-Tran K.L., Ding T., Osteen K.G. Dioxin and endometrial progesterone resistance. Semin Reprod Med 2010, 28:59-68.
12. Igarashi T.M., Bruner-Tran K.L., Yeaman G.R., Lessey B.A., Edwards D.P., Eisenberg E., et al. Reduced expression of progesterone receptor-B in the endometrium of women with endometriosis and in cocultures of endometrial cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fertil Steril 2005, 84:67-74.
13. Osteen K.G., Bruner-Tran K.L., Eisenberg E. Reduced progesterone action during endometrial maturation: a potential risk factor for the development of endometriosis. Fertil Steril 2005, 83:529-537.
14. Brown A.G., Leite R.S., Strauss J.F Mechanisms underlying " functional" progesterone withdrawal at parturition. Ann NY Acad Sci 2004, 1034:36-49.
15. Zakar T., Hertelendy F. Progesterone withdrawal: key to parturition. Am J Obstet Gynecol 2007, 196:289-296.
16. Shanker Y.G., Rao A.J. Progesterone receptor expression in the human placenta. Mol Hum Reprod 1999, 5:481-486.
17. Virgo B.B., Bellward G.D. Serum progesterone levels in the pregnant and postpartum laboratory mouse. Endocrinology 1974, 95:1486-1490.
18. Ogle T.F. Progesterone-action in the decidual mesometrium of pregnancy. Steroids 2002, 67:1-14.
19. An B.S., Choi K.C., Lee G.S., Leung P.C., Jeung E.B. Complex regulation of calbindin-D(9k) in the mouse placenta and extra-embryonic membrane during mid- and late pregnancy. Mol Cell Endocrinol 2004, 214(February (1-2)):39-52.
20. Mendelson C.R. Minireview: fetal-maternal hormonal signaling in pregnancy and labor. Mol Endocrinol 2009, 23:947-954.
21. Wegmann T.G., Lin H., Guilbert L., Mosmann T.R. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon?. Immunol Today 1993, 14:353-356.
22. Challis J.R., Lockwood C.J., Myatt L., Norman J.E., Strauss J.F., Petraglia F. Inflammation and pregnancy. Reprod Sci 2009, 16:206-215.
23. Su L., Sun Y., Ma F., Lü P., Huang H., Zhou J. Progesterone inhibits toll-like receptor 4-mediated innate immune response in macrophages by suppressing NF-kappaB activation and enhancing SOCS1 expression. Immunol Lett 2009, 125:151-155.
24. Elovitz M.A., Wang Z., Chien E.K., Rychlik D.F., Phillippe M. A new model for inflammation-induced preterm birth: the role of platelet-activating factor and toll-like receptor-4. Am J Pathol 2003, 163:2103-2111.
25. Briscoe T., Duncan J., Cock M., Choo J., Rice G., Harding R., et al. Activation of NF-kappaB transcription factor in the preterm ovine brain and placenta after acute LPS exposure. J Neurosci Res 2006, 83:567-574.
26. Lappas M., Yee K., Permezel M., Rice G.E., Lipopolysaccharide TNF-alpha activate the nuclear factor kappa B pathway in the human placental JEG-3 cells. Placenta 2006, 27:568-575.
27. Guo S.W. Nuclear factor-kappab (NF-kappaB): an unsuspected major culprit in the pathogenesis of endometriosis that is still at large?. Gynecol Obstet Invest 2007, 63:71-97.
28. Patni S., Flynn P., Wynen L.P., Seager A.L., Morgan G., White J.O., et al. An introduction to toll-like receptors and their possible role in the initiation of labour. Br J Obstet Gynecol 2007, 114:1326-1334.
29. Faye-Petersen O.M. The placenta in preterm birth. J Clin Pathol 2008, 61:1261-1275.
30. Houben M.L., Nikkels P.G., van Bleek G.M., Visser G.H., Rovers M.M., Kessel H., et al. The association between intrauterine inflammation and spontaneous vaginal delivery at term: a cross-sectional study. PLoS One 2009, 4:e6572.
31. Zarember K.A., Godowski P.J. Tissue expression of human toll-like receptors and differential regulation of toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 2002, 168:554-561.
32. Nishimura M., Naito S. Tissue-specific mRNA expression profiles of human toll-like receptors and related genes. Biol Pharm Bull 2005, 28:886-892. [CrossRef, PubMed Savitz DA, Murnane P. Behavioral influences on preterm birth: a review. Epidemiology 2010 May;21(3):291-9].
33. Mitsunari M., Yoshida S., Shoji T., Tsukihara S., Iwabe T., Harada T., et al. Macrophage-activating lipopeptide-2 induces cyclooxygenase-2 and prostaglandin E(2) via toll-like receptor 2 in human placental trophoblast cells. J Reprod Immunol 2006, 72:46-59. [CrossRef, PubMed].
34. Holmlund U., Cebers G., Dahlfors A.R., Sandstedt B., Bremme K., Ekström E.S., et al. Expression and regulation of the pattern recognition receptors toll-like receptor-2 and toll-like receptor-4 in the human placenta. Immunology 2002, 107:145-151.
35. Kajii T., Ohama K. Androgenetic origin of hydatidiform mole. Nature 1977, 268:633-634.
36. Barton S.C., Surani M.A., Norris M.L. Role of paternal and maternal genomes in mouse development. Nature 1984, 311:374-376.
37. Ishimura R., Ohsako S., Kawakami T., Sakaue M., Aoki Y., Tohyama C. Altered protein profile and possible hypoxia in the placenta of 2,3,7,8-tetrachlorodibenzo-p-dioxin-exposed rats. Toxicol Appl Pharmacol 2002, 185:197-206.
38. Ishimura R., Ohsako S., Miyabara Y., Sakaue M., Kawakami T., Aoki Y., et al. Increased glycogen content and glucose transporter 3 mRNA level in the placenta of Holtzman rats after exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 2002, 178:161-171.
39. Khera K.S. Extraembryonic tissue changes induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin and 2,3,4,7,8-pentachlorodibenzofuran with a note on direction of maternal blood flow in the labyrinth of C57BL/6N mice. Teratology 1992, 45:611-627.
40. Vogel C.F., Zhao Y., Wong P., Young N.F., Matsumura F. The use of c-src knockout mice for the identification of the main toxic signaling pathway of TCDD to induce wasting syndrome. J Biochem Mol Toxicol 2003, 17:305-315.
41. Lanman J.T., Seidman L. Length of gestation in mice under a 21-hour day. Biol Reprod 1977, 17:224-227.
42. Wang H., Xie H., Dey S.K. Loss of cannabinoid receptor CB1 induces preterm birth. PLoS ONE 2008, 3(10):e3320.
43. Roizen J.D., Asada M., Tong M., Tai H.H., Muglia L.J. Preterm birth without progesterone withdrawal in 15-hydroxyprostaglandin dehydrogenase hypomorphic mice. Mol Endocrinol 2008, 22:105-112.
44. Environmental Working Group. Body burden: the pollution in newborns. 2007, available from:, [cited, August 6, 2010]. http://www.ewg.org/reports/bodyburden2/.
45. White S.S., Birnbaum L.S. An overview of the effects of dioxins and dioxin-like compounds on vertebrates, as documented in human and ecological epidemiology. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2009, 27:197-211.
46. Homberger E., Reggiani G., Sambeth J., Wipf H.K. The Seveso accident: its nature. Extent and consequences. Ann Occup Hyg 1979, 22:327-370.
47. Eskenazi B., Mocarelli P., Warner M., Samuels S., Vercellini P., Olive D., et al. Seveso Women's Health Study: a study of the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on reproductive health. Chemosphere 2000, 40:1247-1253.
48. Eskenazi B., Mocarelli P., Warner M., Chee W.Y., Gerthoux P.M., Samuels S., et al. Maternal serum dioxin levels and birth outcomes in women of Seveso, Italy. Environ Health Perspect 2003, 111:947-953.
49. Michalek J.E., Rahe A.J., Boyle C.A. Paternal dioxin, preterm birth, intrauterine growth retardation, and infant death. Epidemiology 1998, 9(March (2)):161-167.
50. Lawson C.C., Schnorr T.M., Whelan E.A., Deddens J.A., Dankovic D.A., Piacitelli L.A., et al. Paternal occupational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin and birth outcomes of offspring: birth weight, preterm delivery, and birth defects. Environ Health Perspect 2004, 112:1403-1408.
51. Le T.N., Johansson A. Impact of chemical warfare with agent orange on women's reproductive lives in Vietnam: a pilot study. Reprod Health Matters 2001, 9:156-164.
52. Lappas M., Rice G.E. Transcriptional regulation of the processes of human labour and delivery. Placenta 2009, 30:S90-S95.
53. King A.E., Critchley H.O., Kelly R.W. The NF-kappaB pathway in human endometrium and first trimester decidua. Mol Hum Reprod 2001, 7:175-183.
54. Liu H., Redline R.W., Han Y.W. Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J Immunol 2007, 179:2501-2508.
55. Cookson V.J., Chapman N.R. NF-kappaB function in the human myometrium during pregnancy and parturition. Histol Histopathol 2010, 25(7):945-956.
56. Lisonkova S., Janssen P.A., Sheps S.B., Lee S.K., Dahlgren L. The effect of maternal age on adverse birth outcomes: does parity matter?. J Obstet Gynaecol Can 2010, 32:541-548.
57. Chen X.K., Wen S.W., Krewski D., Fleming N., Yang Q., Walker M.C. Paternal age and adverse birth outcomes: teenager or 40+, who is at risk?. Hum Reprod 2008, 23:1290-1296.
58. Mocchegiani E., Corsonello A., Lattanzio F. Frailty ageing and inflammation: reality and perspectives. Biogerontology 2010, August 18 [Epub ahead of print].
59. Wolkowitz O.M., Epel E.S., Reus V.I., Mellon S.H. Depression gets old fast: do stress and depression accelerate cell aging?. Depress Anxiety 2010, 27(4):327-338.
60. Dolinoy D.C., Weidman J.R., Jirtle R.L. Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod Toxicol 2007, 23:297-307.
61. Gluckman P.D., Hanson M.A., Cooper C., Thornburg K.L. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008, 359:61-73.