Effects of cadmium on the expression of placental lactogens and Pit-1 genes in the rat placental trophoblast cells

Molecular and Cellular Endocrinology

Volumn 298, Issue 1-2, 2009, Pages 11-18

  Lee, Chae Kwan ^a   Lee, Jong Tae ^a   Yu, Seong Jin ^b   Kang, Sung Goo ^b   Moon, Chan Seok ^c   Choi, Young Ha ^b   Kim, Jeong Ho ^a   Kim, Dae Hwan ^a   Son, Byung Chul ^a   Lee, Chang Hee ^a   Kim, Hwi Dong ^a   Ahn, Jin Hong ^a  

^a Inje University College of Medicine   (South Korea)

^b Inje University   (South Korea)

^c Catholic University of Pusan   (South Korea)

Author keywords

Cadmium; Pit 1; Placenta; Placental lactogen; Trophoblast cells

Indexed keywords

CADMIUM; ESTROGEN; MESSENGER RNA; PROLACTIN; SODIUM CHLORIDE; TRANSCRIPTION FACTOR PIT 1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA FRAGMENTATION; IMMUNOHISTOCHEMISTRY; NONHUMAN; NORTHERN BLOTTING; PLACENTA; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOBLAST;

ANIMALS; CADMIUM; CELL COUNT; DOWN-REGULATION; EMBRYO IMPLANTATION; FEMALE; FETAL VIABILITY; GENE EXPRESSION REGULATION; PLACENTA; PLACENTAL LACTOGEN; PREGNANCY; PROLACTIN; RATS; RATS, INBRED F344; TRANSCRIPTION FACTOR PIT-1; TROPHOBLASTS;

EID: 57749177920     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.09.028     Document Type: Article

References (83)

1. Adams S.O., Nissley S.P., Kasuga M., Foley T.P., and Rechler M.M. Receptors for insulin-like growth factors and growth effects of multiplication-stimulating activity (rat insulin-like growth factor II) in rat embryo fibroblasts. Endocrinology 112 (1983) 971-978
2. Ain R., Dai G., Dunmore J.H., Godwin A.R., and Soares M.J. A prolactin family paralog regulates reproductive adaptations to a physiological stressor. Proc. Natl. Acad. Sci. U.S.A. 23 (2004) 16543-16548
3. Angerer L.M., Cox K.H., and Angerer R.C. Demonstration of tissue-specific gene expression by in situ hybridization. Methods Enzymol. 152 (1987) 649-661
4. Anthony R.V., Pratt S.L., Liang R., and Holland M.D. Placental-fetal hormonal interactions: impact on fetal growth. J. Anim. Sci. 73 (1995) 1861-1871
5. Balasinor N., Gill-Sharma M.K., Parte P., D'Souza S., Kedia N., and Juneja H.S. Effects of paternal administration of an antiestrogen, tamoxifen, on embryo development in rats. Mol. Cell. Endocrinol. 190 (2002) 159-166
6. Bamberger A.M., Bamberger C.M., Pu L.P., Puy L.A., Loh Y.P., and Asa S.L. Expression of pit-1 messenger ribonucleic acid and protein in the human placenta. J. Clin. Endocrinol. Metab. 80 (1995) 2021-2026
7. Bhattachayya M.H., Wilson A.K., Rajin S.S., and Jonah M. Biochemical pathways in cadmium toxicity. In: Zalup R.K., and Koropatnick J. (Eds). Molecular Biology and Toxicology of Metals (2000), Taylor and Francis, London 1-74
8. Bodner M., Castrillo J.L., Theill L.E., Deerinck T., Ellisman M., and Karin M. The pituitary-specific transcription factor GHF-1 is a homeobox-containing protein. Cell 55 (1988) 505-518
9. Briz O., el-Mir M.Y., Bravo P., Villanueva G.R., and Marin J.J. Fetal excretion of the fluorescent bile acid derivative cholylglycylamido-fluorescein (FITC-GC) by the rat placenta-maternal liver tandem. Placenta 19 (1998) 119-126
10. Bush P.G., Mayhew T.M., Abramovich D.R., Aggett P.J., Burke M.D., and Page K.R. A quantitative study on the effects of maternal smoking on placental morphology and cadmium concentration. Placenta 21 (2000) 247-256
11. Byatt J.C., Eppard P.J., Munyakazi L., Sorbet R.H., Veenhuizen J.J., Curran D.F., and Collier R.J. Stimulation of milk yield and feed intake by bovine placental lactogen in the dairy cow. J. Dairy Sci. 75 (1992) 1216-1223
12. Byatt J.C., Eppard P.J., Veenhuizen J.J., Sorbet R.H., Buonomo F.C., Curran D.F., and Collier R.J. Serum half-life and in-vivo actions of recombinant bovine placental lactogen in the dairy cow. J. Endocrinol. 132 (1992) 185-193
13. Campbell W.J., Deb S., Kwok S.C., Joslin J.A., and Soares M.J. Differential expression of placental lactogen-II and prolactin-like protein-A in the rat chorioallantoic placenta. Endocrinology 125 (1989) 1565-1574
14. Cohick C.B., Dai G., Xu L., Deb S., Kamei T., Levan G., Szpirer C., Szpirer J., Kwok S.C., and Soares M.J. Placental lactogen-I variant utilizes the prolactin receptor signaling pathway. Mol. Cell. Endocrinol. 116 (1996) 49-58
15. Conliffe P.R., Simmen R.C.M., Buhi W.C., and Shiverick K.T. Cloning of a novel rat placental prolactin-like protein C-related cDNA. Mol. Reprod. Dev. 41 (1995) 167-176
16. Croze F., Kennedy T.G., Schroedter I.C., and Friesen H.G. Expression of rat prolactin-like protein B in deciduoma of pseudopregnant rat and in decidua during early pregnancy. Endocrinology 127 (1990) 2665-2672
17. Deb S., Faria T.N., Roby K.F., Larsen D., Kwok S.C., Talamantes F., and Soares M.J. Identification and characterization of a new member of the prolactin family, placental lactogen-I variant. J. Biol. Chem. 266 (1991) 1605-1610
18. Deb S., Roby K.F., Faria T.N., Szpirer C., Levan G., Kwok S.C.M., and Soares M.J. Molecular cloning and characterization of prolactin-like protein C complementary deoxyribonucleic acid. J. Biol. Chem. 266 (1991) 23027-23032
19. Di Sant'Agnese P.A., Jensen K.D., Levin A., and Miller R.K. Placental toxicity of cadmium in the rat: an ultrastructural study. Placenta 4 (1983) 149-163
20. Duckworth M.L., Kirk K.L., and Friesen H.G. Isolation and identification of a cDNA clone of rat placental lactogen II. J. Biol. Chem. 261 (1986) 10871-10878
21. Duckworth M.L., Peden L.M., and Friesen H.G. Isolation of a novel prolactin-like cDNA clone from developing rat placenta. J. Biol. Chem. 261 (1986) 10879-10884
22. Elsholtz H.P., Lew A.M., Albert P.R., and Sundmark V.C. Inhibitory control of prolactin and Pit-1 promoters by dopamine. Dual signaling pathways required for D2 receptor-regulated expression of the prolactin gene. J. Biol. Chem. 266 (1991) 22919-22925
23. Ema M., and Harazono A. Adverse effects of dibutyltin dichloride on initiation and maintenance of rat pregnancy. Reprod. Toxicol. 14 (2000) 451-456
24. Ferm V.H. Developmental malformations induced by cadmium. A study of timed injections during embryogenesis. Biol. Neonate 19 (1971) 101-107
25. Freemark M., Kirk K., Pihoker C., Robertson M.C., Shiu R.P., and Driscoll P. Pregnancy lactogens in the rat conceptus and fetus: circulating levels, distribution of binding, and expression of receptor messenger ribonucleic acid. Endocrinology 133 (1993) 1830-1842
26. Garcia-Morales P., Saceda M., Kenney N., Kim N., Salomon D.S., Gottardis M.M., Solomon H.B., Sholler P.F., Jordan V.C., and Martin M.B. Effect of cadmium on estrogen receptor levels and estrogen-induced responses in human breast cancer cells. J. Biol. Chem. 269 (1994) 16896-16901
27. Gil-Puig C., Seoane S., Blanco M., Macia M., Garcia-Caballero T., Segura C., and Perez-Fernandez R. Pit-1 is expressed in normal and tumorous human breast and regulates GH secretion and cell proliferation. Eur. J. Endocrinol. 153 (2005) 335-344
28. Hamlin G.P., Lu X.J., Roby K.F., and Soares M.J. Recapitulation of the pathway for trophoblast giant cell differentiation in vitro: stage-specific expression of members of the prolactin gene family. Endocrinology 134 (1994) 2390-2396
29. Haugen B.R., Wood W.M., Gordon D.F., and Ridgway E.C. A thyrotrope-specific variant of Pit-1 transactivates the thyrotropin beta promoter. J. Biol. Chem. 268 (1993) 20818-20824
30. Henson M.C., and Anderson M.B. The effects of cadmium on placental endocrine function. Recent Res. Dev. Endocrinol. 1 (2000) 37-47
31. Henson M.C., and Chedrese P.J. Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp. Biol. Med. 229 (2004) 383-392
32. Ho-Chen J.K., Bustamante J.J., and Soares M.J. Prolactin-like protein-f subfamily of placental hormones/cytokines: responsiveness to maternal hypoxia. Endocrinology 148 (2007) 559-565
33. Ingraham H.A., Albert V.R., Chen R.P., Crenshaw III E.B., Elsholtz H.P., He X., Kapiloff M.S., Mangalam H.J., Swanson L.W., and Treacy M.N. A family of POU-domain and Pit-1 tissue-specific transcription factors in pituitary and neuroendocrine development. Annu. Rev. Physiol. 52 (1990) 773-791
34. Ingraham H.A., Chen R.P., Mangalam H.J., Elsholtz H.P., and Flynn S.E. A tissue-specific transcription factor containing a homeodomain specifies a pituitary phenotype. Cell 55 (1988) 519-529
35. Ishitobi H., Mori K., Yoshida K., and Watanabe C. Effects of perinatal exposure to low-dose cadmium on thyroid hormone-related and sex hormone receptor gene expressions in brain of offspring. Neurotoxicology 28 (2007) 790-797
36. Iwatzuki K., Shinozaki M., Hattori N., Hirasawa K., Itagaki S.I., Shita K., and Ogawa T. Molecular cloning and characterization of a new member of the rat placental prolactin (PRL) family, PRL-like protein D (PLP-D). Endocrinology 137 (1996) 3849-3855
37. Jarup L., Berglund M., Elinder C.G., Nordberg G., and Vahter M. Health effects of cadmium exposure-a review of the literature and a risk estimate. Scand. J. Work Environ. Health 24 (1998) 1-51
38. Johnson M.D., Kenney N., Stoica A., Hilakivi-Clarke L., Singh B., Chepko G., Clarke R., Sholler P.F., Lirio A.A., Foss C., Reiter R., Trock B., Paik S., and Martin M.B. Cadmium mimics the in vivo effects of estrogen in the uterus and mammary gland. Nat. Med. 9 (2003) 1081-1084
39. Kawai M., and Kishi K. In vitro studies of the stimulation of insulin secretion and B-cell proliferation by rat placental lactogen-II during pregnancy in rats. J. Reprod. Fert. 109 (1997) 145-152
40. Konzak K.E., and Moore D.D. Functional isoforms of Pit-1 generated by alternative messenger RNA splicing. Mol. Endocrinol. 6 (1992) 241-247
41. Lacroix M.C., Devinoy E., Cassy S., Servely J.L., Vidaud M., and Kann G. Expression of growth hormone and its receptor in the placental and feto-maternal environment during early pregnancy in sheep. Endocrinology 140 (1999) 5587-5597
42. Larsen L.G., Clausen H.V., and Jønsson L. Stereologic examination of placentas from mothers who smoke during pregnancy. Am. J. Obstet. Gynecol. 186 (2002) 531-537
43. Lee B.J., Jeong J.K., Kim J.H., Kang S.G., Kim M.O., and Choi W.S. Local expression of a POU family transcription factor, Pit-1, in the rat placenta. Mol. Cell. Endocrinol. 118 (1996) 9-14
44. Lee B.J., Kim J.H., Lee C.K., Kang H.M., Kim H.C., and Kang S.G. Changes in mRNA levels of a pituitary-specific trans-acting factor, Pit-1, and prolactin during the rat estrous cycle. Eur. J. Endocrinol. 132 (1995) 771-776
45. Lee C.K., Kim S.H., Moon D.H., Kim J.H., Son B.C., Kim D.H., Lee C.H., Kim H.D., Kim J.W., Kim J.E., and Lee C.U. Effects of bisphenol A on the placental function and reproduction in rats. J. Prev. Med. Pub. Health. 38 (2005) 330-336
46. Lee C.K., Kang H.S., Lee B.J., Kang H.M., Choi W.S., and Kang S.G. Effects of dopamine and estrogen on the regulation of Pit-1α, Pit-1, and PL-II gene expression in the rat placenta. Mol. Cells 8 (1998) 205-211
47. Lemaigre F.P., Peers B., Lafontaine D.A., Mathy-Hartert M., Rousseau G.G., Belayew A., and Martial J.A. Pituitary-specific factor binding to the human prolactin, growth hormone, and placental lactogen genes. DNA 8 (1989) 149-159
48. Levin A.A., Plautz J.R., di Sant'Agnese P.A., and Miller R.K. Cadmium: placental mechanisms of fetal toxicity. Placenta Suppl. 3 (1981) 303-318
49. Li S., Crenshaw III E.B., Rawson E.J., Simmons D.M., Swanson L.W., and Rosenfeld M.G. Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene pit-1. Nature 347 (1990) 528-533
50. Massanyi P., Uhrin V., Sirotkin A.V., Paksy K., Foracs Z.S., Toman R., and Kovacik J. Effects of cadmium on ultrastructure and streoidogenesis in cultured porcine ovarian granulose cells. Acta. Vet. Brno. 69 (2000) 101-106
51. Matsuura S., Itakura A., Ohno Y., Nakashima Y., Murata Y., Takeuchi M., Kobayashi M., and Mizutani S. Effects of estradiol administration on feto-placental growth in rat. Early Hum. 77 (2004) 47-56
52. McTernan C.L., Draper N., Nicholson H., Chalder S.M., Driver P., Hewison M., Kilby M.D., and Stewart P.M. Reduced placental 11betahydroxysteroid dehydrogenase type 2 mRNA levels in human pregnancies complicated by intrauterine growth restriction: an analysis of possible mechanisms. J. Clin. Endocrinol. Metab. 86 (2001) 4979-4983
53. Min S.H., Mackenzie D.D., Breier B.H., McCutcheon S.N., and Gluckman P.D. Growth-promoting effects of ovine placental lactogen (oPL) in young lambs: comparison with bovine growth hormone provides evidence for a distinct effect of oPL on food intake. Growth Regul. 6 (1996) 144-151
54. Miyai S., Yoshimura S., Iwasaki Y., Takekoshi S., Lloyd R.V., and Osamura R.Y. Induction of GH, PRL, and TSH beta mRNA by transfection of Pit-1 in a human pituitary adenoma-derived cell line. Cell Tissue Res. 322 (2005) 269-277
55. Morris A.E., Kloss B., McChesney R.E., Bancroft C., and Chasin L.A. An alternatively spliced Pit-1 isoform altered in its ability to trans-activate. Nucleic Acids Res. 20 (1992) 1355-1361
56. Nesatyy V.J., Ammann A.A., Rutishauser B.V., and Suter M.J. Effect of cadmium on the interaction of 17beta-estradiol with the rainbow trout estrogen receptor. Environ. Sci. Technol. 40 (2006) 1358-1363
57. Nesatyy V.J., Rutishauser B.V., Eggen R.I., and Suter M.J. Identification of the estrogen receptor Cd-binding sites by chemical modification. Analyst 130 (2005) 1087-1097
58. Nishijo M., Tawara K., Honda R., Nakagawa H., Tanebe K., and Saito S. Relationship between newborn size and mother's blood cadmium levels, Toyama, Japan. Arch. Environ. Health 59 (2004) 22-25
59. Oztürk A., Donald L.J., Li L., Duckworth H.W., and Duckworth M.L. Proteomic identification of AP2 gamma as a rat placental lactogen II trophoblast cell-specific enhancer binding protein. Endocrinology 147 (2006) 4319-4329
60. Palanza P., Parmigiani S., and vom Saal F.S. Effects of prenatal exposure to low doses of diethylstilbestrol, o,p'DDT, and methoxychlor on postnatal growth and neurobehavioral development in male and female mice. Horm. Behav. 40 (2001) 252-265
61. Pellegrini I., Roche C., Quentien M.H., Ferrand M., Gunz G., Thirion S., Bagnis C., Enjalbert A., and Franc J.L. Involvement of the pituitary-specific transcription factor pit-1 in somatolactotrope cell growth and death: an approach using dominant-negative pit-1 mutants. Mol. Endocrinol. 20 (2006) 3212-3227
62. Piasek M., Blanusa M., Kostial K., and Laskey J.W. Placental cadmium and progesterone concentrations in cigarette smokers. Reprod. Toxicol. 15 (2001) 673-681
63. Reid G.J., Flozak A.S., and Simmons R.A. Placental expression of insulin-like growth factor receptor-1 and insulin receptor in the growth-restricted fetal rat. J. Soc. Gynecol. Investig. 9 (2002) 210-214
64. Robertson M.C., Croze F., Schroedter I.C., and Friesen H.G. Molecular cloning and expression of rat placental lactogen-I complementary deoxyribonucleic acid. Endocrinology 127 (1990) 702-710
65. Robertson M.C., Gillespie B., and Friesen H.G. Characterization of the two forms of rat placental lactogen (rPL): rPL-I and rPL-α. Endocrinology 111 (1982) 1862-1866
66. Roby K.F., Deb S., Gibori G., Szpirer C., Levan G., Kwok S.C.M., and Soares M.J. Decidual prolactin-related protein. J. Biol. Chem. 268 (1993) 3316-3342
67. Roby K.F., and Soares M.J. Trophoblast cell differentiation and organization: role of fetal and ovarian signals. Placenta 14 (1993) 529-545
68. Saltzman R.A., Miller R.K., and di Sant'Agnese P.A. Cadmium exposure on day 12 of gestation in the Wistar rat: distribution, uteroplacental blood flow, and fetal viability. Teratology 39 (1989) 19-30
69. Schoknecht P.A., McGuire M.A., Cohick W.S., Currie W.B., and Bell A.W. Effect of chronic infusion of placental lactogen on ovine fetal growth in late gestation. Domest. Anim. Endocrinol. 13 (1996) 519-528
70. Schoknecht P.A., Nobrega S.N., Petterson J.A., Ehrhardt R.A., Slepetis R., and Bell A.W. Relations between maternal and fetal plasma concentrations of placental lactogen and placental and fetal weights in well-fed ewes. J. Anim. Sci. 69 (1991) 1059-1063
71. Soares M.J., Muller H., Orwig K.E., Peters T.J., and Dai G. The uteroplacental prolactin family and pregnancy. Biol. Repod. 58 (1998) 273-284
72. Sun Y., and Duckworth M.L. Identification of a placental-specific enhancer in the rat placental lactogen II gene that contains binding sites for members of the Ets and AP-1 (activator protein 1) families of transcription factors. Mol. Endocrinol. 13 (1999) 385-399
73. Takiguchi M., and Yoshihara S. New aspects of cadmium as endocrine disruptor. Environ. Sci. 13 (2006) 107-116
74. Taylor M.J., Jenkin G., Robinson J.S., Thorburn G.D., Friesen H., and Chan J.S. Concentrations of placental lactogen in chronically catheterized ewes and fetuses in late pregnancy. J. Endocrinol. 85 (1980) 27-34
75. Telleria C.M., Zhong L., Deb S., Srivastava R.K., Park K.S., Sugino N., Park-Sarge O.K., and Gibori G. Differential expression of the estrogen receptors alpha and beta in the rat corpus luteum of pregnancy: regulation by prolactin and placental lactogens. Endocrinology 139 (1998) 2432-2442
76. Tennekoon K.H., Pathmaperuma A.N., Senanayake L., and Karunanayake E.H. Insulin-like growth factors-I and -II and insulin-like growth factor binding protein-1 during normal pregnancy: pattern of secretion and correlation with other placental hormones. Ceylon. Med. J. 52 (2007) 8-13
77. Theill L.E., Hattori K., Lazzaro D., Castrillo J.L., and Karin M. Differential splicing of the GHF1 primary transcript gives rise to two functionally distinct homeodomain proteins. EMBO J. 11 (1992) 2261-2269
78. Tyl R.W., Marr M.C., Myers C.B., Ross W.P., and Friedman M.A. Relationship between acrylamide reproductive and neurotoxicity in male rats. Reprod. Toxicol. 14 (2000) 147-157
79. Varga B., Zsolnai B., Paksy K., Náray M., and Ungváry G. Age dependent accumulation of cadmium in the human ovary. Reprod. Toxicol. 7 (1993) 225-228
80. Ward R.D., Stone B.M., Raetzman L.T., and Camper S.A. Cell proliferation and vascularization in mouse models of pituitary hormone deficiency. Mol. Endocrinol. 20 (2006) 1378-1390
81. Yamada T., Hara M., Ohba Y., Inoue T., and Ohno H. Studies on implantation traces in rats. II. Staining of cleared uteri, formation and distribution of implantation treces. Exp. Anim. 34 (1985) 249-260
82. Yang K., Julan L., Rubio F., Sharma A., and Guan H. Cadmium reduces 11 beta-hydroxysteroid dehydrogenase type 2 activity and expression in human placental trophoblast cells. Am. J. Physiol. Endocrinol. Metab. 290 (2006) 135-142
83. Zadorozhnaja T.D., Little R.E., Miller R.K., Mendel N.A., Taylor R.J., Presley B.J., and Gladen B.C. Concentrations of arsenic, cadmium, copper, lead, mercury, and zinc in human placentas from two cities in Ukraine. J. Toxicol. Environ. Health A 61 (2000) 255-263