Evidence of steroid hormone activity in the chorioallantoic membrane of a Turtle (Pseudemys nelsoni)

General and Comparative Endocrinology

Volumn 186, Issue , 2013, Pages 50-57

  Cruze, Lori ^a,d   Hamlin, Heather J ^b,d   Kohno, Satomi ^a,d   McCoy, Michael W ^c,d   Guillette, Louis J ^a,d  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF MAINE   (United States)

^c EAST CAROLINA UNIVERSITY   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

Amniotes; Endocrine activity; Evolution of viviparity; Extraembryonic membranes

Indexed keywords

ANDROGEN; ESTROGEN RECEPTOR; PROGESTERONE; PROGESTERONE RECEPTOR; RNA; STEROID HORMONE; STEROID RECEPTOR;

ANIMAL TISSUE; ARTICLE; CHORIOALLANTOIS; CONTROLLED STUDY; EMBRYO; EXPLANT; FEMALE; GENE EXPRESSION; HORMONE ACTION; HORMONE SYNTHESIS; IN VITRO STUDY; INCUBATION TEMPERATURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PSEUDEMYS NELSONI; RNA TRANSLATION; TURTLE;

EID: 84875764657     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2013.02.007     Document Type: Article

References (57)

1. Hormones and Reproduction in Vertebrates 2011, vol. 3:247-275. Elsevier.
2. Albergotti L.C., Hamlin H.J., McCoy M.W., Guillette L.J. Endocrine activity of extraembryonic membranes extends beyond placental amniotes. PLoS ONE 2009, 4:e5452.
3. Ancelin M., Buteau-Lozano H., Meduri G., Osborne-Pellegrin M., Sordello S., Plouët J., Perrot-Applanat M. A dynamic shift of VEGF isoforms with a transient and selective progesterone-induced expression of VEGF189 regulates angiogenesis and vascular permeability in human uterus. Proc. Natl. Acad. Sci. USA 2002, 99:6023-6028.
4. Andrews R.M., Mathies T. Natural history of reptilian development: constraints on the evolution of viviparity. Bioscience 2000, 50:227-238.
5. Arensburg J., Payne A.H., Orly J. Expression of steroidogenic genes in maternal and extraembryonic cells during early pregnancy in mice. Endocrinology 1999, 140:5220-5232.
6. Blackburn D.G. Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. Am. Zool. 1992, 32:313-321.
7. Blackburn D.G. Viviparity and oviparity: evolution and reproductive strategies. Encyclopedia of Reproduction 1999, vol. 4:994-1003. Academic Press, London, UK.
8. Callard I.P., Lance V., Salhanick A.R., Barad D. The annual ovarian cycle of Chrysemys picta: Correlated changes in plasma steroids and parameters of vitellogenesis. Gen. Comp. Endocrinol. 1978, 35:245-257.
9. Chan C.C.W., Lao T.T., Ho P.C., Sung E.O.P., Cheung A.N.Y. The effect of mifepristone on the expression of steroid hormone receptors in human decidua and placenta: a randomized placebo-controlled double-blind study. J. Clin. Endocrinol. Metab. 2003, 88:5846-5850.
10. Cree A., Guillette L.J., Reader K. Eggshell formation during prolonged gravidity of the tuatara Sphenodon punctatus. J. Morphol. 1996, 230:129-144.
11. Cross J.C., Baczyk D., Dobric N., Hemberger M., Hughes M., Simmons D.G., Yamamoto H., Kingdom J.C.P. Genes, development and evolution of the placenta. Placenta 2003, 123-130.
12. Cruze L., Kohno S., McCoy M.W., Guillette L.J. Towards an understanding of the evolution of the chorioallantoic placenta: steroid biosynthesis and steroid hormone signaling in the chorioallantoic membrane of an oviparous reptile. Biol. Reprod. 2012, 87:71, 71-11.
13. Cudeville C., Mondon F., Robert B., Rebourcet R., Mignot T.-M., Benassayag C., Ferre F. Evidence for progesterone receptors in the human fetoplacental vascular tree. Biol. Reprod. 2000, 62:759-765.
14. Durkee T.J., McLean M.P., Hales D.B., Payne A.H., Waterman M.R., Khan I., Gibori G. P450(17 alpha) and P450SCC gene expression and regulation in the rat placenta. Endocrinology 1992, 130:1309-1317.
15. Enge K.M., Percival H.F., Rice K.G., Jennings M.L., Masson G.R., Woodward A.R. Summer nesting of turtles in alligator nests in Florida. J. Herpetol. 2000, 34:497-503.
16. Ewert M.A., Etchberger C.R., Nelson C.E. Turtle sex-determining modes and TSD patterns, and some TSD patterns correlates. Temperature-Dependent Sex Determination 2004, 21-32. Smithsonian Books. N. Valenzuela, J.J. Bull (Eds.).
17. Ezaz T., Stiglec R., Veyrunes F., Marshall Graves J.A. Relationships between vertebrate ZW and XY sex chromosome systems. Curr. Biol. 2006, 16:R736-R743.
18. Ferguson M. Reproductive biology and embryology of the crocodilians. Biology of the Reptilia 1985, vol. 14:329-491. J. Wiley and Sons, New York.
19. Fujimoto J., Nakagawa Y., Toyoki H., Sakaguchi H., Sato E., Tamaya T. Estrogen-related receptor expression in placenta throughout gestation. J. Steroid Biochem. Mol. Biol. 2005, 94:67-69.
20. Giannoulias D., Haluska G.J., Gravett M.G., Sadowsky D.W., Challis J.R.G., Novy M.J. Localization of prostaglandin H synthase, prostaglandin dehydrogenase, corticotropin releasing hormone and glucocorticoid receptor in rhesus monkey fetal membranes with labor and in the presence of infection. Placenta 2005, 26:289-297.
21. Girling J.E., Jones S.M. In vitro progesterone production by maternal and embryonic tissues during gestation in the southern snow skink (Niveoscincus microlepidotus). Gen. Compd. Endocrinol. 2003, 133:100-108.
22. Guillette L.J., Spielvogel S., Moore F.L. Luteal development, placentation, and plasma progesterone concentration in the viviparous lizard Sceloporus jarrovi. Gen. Compd. Endocrinol. 1981, 43:20-29.
23. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morphol. 1951, 88:49-92.
24. Hsu T.Y., Lan K.C., Tsai C.C., Ou C.Y., Cheng B.H., Tsai M.Y., Kang H.Y., Tung Y.H., Wong Y.H., Huang K.E. Expression of androgen receptor in human placentas from normal and preeclamptic pregnancies. Taiwan J. Obstet. Gyne. 2009, 48:262-267.
25. Jojovic M., Wolf F., Mangold U. Epidermal growth factor, vascular endothelial growth factor and progesterone promote placental development in rat whole-embryo culture. Anat. Embryol. (Berl) 1998, 198:133-139.
26. King S.R., Matassa A.A., White E.K., Walsh L.P., Rao R.M., Stocco D.M., Reyland M.E. Oxysterols regulate expression of the steroidogenic acute regulatory protein. J. Mol. Endocrinol. 2004, 32:507-517.
27. Levitz M. Conjugation and transfer of fetal-placental steroid hormones. J. Clin. Endocrinol. Metab. 1966, 26:773-777.
28. Mark P.J., Smith J.T., Waddell B.J. Placental and fetal growth retardation following partial progesterone withdrawal in rat pregnancy. Placenta 2006, 27:208-214.
29. McCoy K.A., Bortnick L.J., Campbell C.M., Hamlin H.J., Guillette L.J.J., Mary C.M.St. Agriculture alters gonadal form and function in the toad Bufo marinus. Environ. Health Perspect. 2008, 116:1526-1532.
30. Mesiano S. Roles of estrogen and progesterone in human parturition. Front. Horm. Res. 2001, 27:86-104.
31. Mesiano S., Chen E.C., Fitter J.T., Kwek K., Yeo G., Smith R. Progesterone withdrawal and estrogen activation in human parturition are coordinated by progesterone receptor a expression in the myometrium. J. Clin. Endocrinol. Metab. 2002, 87:2924-2930.
32. Mess A., Blackburn D.G., Zeller U. Evolutionary transformations of fetal membranes and reproductive strategies. J. Exp. Zool. A 2003, 299A:3-12.
33. Mess A., Carter A.M. Evolution of the placenta during the early radiation of placental mammals. Comp. Biochem. Phys. A 2007, 148:769-779.
34. Mossman H.W. Vertebrate Fetal Membranes: Comparative Ontogeny and Morphology, Evolution, Phylogenetic Significance, Basic Functions, Research Opportunities 1987, vol. xvii. Rutgers University Press, New Brunswick, N.J., 383 pp.
35. Munro H.N., Pilistine S.J., Fant M.E. The Placenta in nutrition. Annu. Rev. Nutr. 1983, 3:97-124.
36. Neill W.T. Viviparity in snakes: some ecological and zoogeographical considerations. Am. Nat. 1964, 98:35-55.
37. Norris D.O. Vertebrate Endocrinology 2007, Academic Press, San Diego.
38. Ogle T.F. Characteristics of high affinity progesterone binding to rat placental cytosol. Endocrinology 1980, 106:1861-1868.
39. Ogle T.F., Mills T.M., Costoff A. Progesterone maintenance of the placental progesterone receptor and placental growth in ovariectomized rats. Biol. Reprod. 1990, 43:276-284.
40. Omar H.A., Ramirez R., Gibson M. Properties of a progesterone-induced relaxation in human placental arteries and veins. J. Clin. Endocrinol. Metab. 1995, 80:370-373.
41. Painter D.L., Moore M.C. Steroid hormone metabolism by the chorioallantoic placenta of the mountain spiny lizard Sceloporus jarrovi as a possible mechanism for buffering maternal-fetal hormone exchange. Physiol. Biochem. Zool. 2005, 78:364-372.
42. Pasqualini J.R. Enzymes involved in the formation and transformation of steroid hormones in the fetal and placental compartments. J. Steroid Biochem. Mol. Biol. 2005, 97:401-415.
43. Payne A.H., Hales D.B. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocrinol. Rev. 2004, 25:947-970.
44. Petraglia F., Florio P., Nappi C., Genazzani A.R. Peptide signaling in human placenta and membranes: autocrine, paracrine, and endocrine mechanisms. Endocrinol. Rev. 1996, 17:156-186.
45. Pieber D., Allport V.C., Hills F., Johnson M., Bennett P.R. Interactions between progesterone receptor isoforms in myometrial cells in human labour. Mol. Hum. Reprod. 2001, 7:875-879.
46. Pinheiro J.C., Bates D.M. Mixed Effects Models in S and S-Plus 2000, Springer.
47. Reynolds L.P., Redmer D.A. Angiogenesis in the placenta. Biol. Reprod. 2001, 64:1033-1040.
48. Ribatti D., Nico B., Vacca A., Roncali L., Burri P.H., Djonov V. Chorioallantoic membrane capillary bed: a useful target for studying angiogenesis and anti-angiogenesis in vivo. Anat. Rec. 2001, 264:317-324.
49. Rider V., Carlone D.L., Foster R.T. Oestrogen and progesterone control basic fibroblast growth factor mRNA in the rat uterus. J. Endocrinol. 1997, 154:75-84.
50. Romanoff A.L. The Avian Embryo 1960, Macmillan, New York.
51. Stewart M.E., Terepka A.R. Transport functions of the chick chorio-allantoic membrane: normal histology and evidence for active electrolyte transport from the allantoic fluid, in vivo. Exp. Cell Res. 1969, 58:93-106.
52. R.D.C. Team, R: A language and environment for statistical computing. R foundation for statistical computing, reference index version 2.15.2. Vienna, Austria, 2008.
53. M.J.Tsai, BW O.M. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 1994, 451-486.
54. Walter L.M., Rogers P.A.W., Girling J.E. The role of progesterone in endometrial angiogenesis in pregnant and ovariectomised mice. Reproduction 2005, 129:765-777.
55. Wilting J., Christ B., Bokeloh M., Weich H.A. In vivo effects of vascular endothelial growth factor on the chicken chorioallantoic membrane. Cell Tissue Res. 1993, 274:163-172.
56. Yntema C.L. A series of stages in the embryonic development of Chelydra serpentina. J. Morphol. 1968, 125:219-251.
57. Zardoya R., Meyer A. The evolutionary position of turtles revised. Naturwissenschaften 2001, 88:193-200.