Developmental programing: Impact of testosterone on placental differentiation

Reproduction

Volumn 148, Issue 2, 2014, Pages 199-209

  Beckett, E M ^a   Astapova, O ^a   Steckler, T L ^a,b   Veiga Lopez, A ^a   Padmanabhan, V ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROSTANOLONE; FLUTAMIDE; ROSIGLITAZONE; TESTOSTERONE; ANDROGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIRTH WEIGHT; COMPARATIVE STUDY; CONTROLLED STUDY; ESTROGEN ACTIVITY; FEMALE; FETUS WEIGHT; GESTATIONAL AGE; INSULIN SENSITIVITY; INTRAUTERINE GROWTH RETARDATION; LOW BIRTH WEIGHT; MALE; NONHUMAN; OVINE MODEL; PLACENTA DEVELOPMENT; PLACENTA FUNCTION; PLACENTA INSUFFICIENCY; PLACENTAL DIFFERENTIATION; PRIORITY JOURNAL; PROGENY; REPRODUCTION; SEX DIFFERENTIATION; TESTOSTERONE SYNTHESIS; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; FETAL GROWTH RETARDATION; INSULIN RESISTANCE; PLACENTA; PREGNANCY; PRENATAL EXPOSURE; SHEEP;

ANDROGENS; ANIMALS; BIRTH WEIGHT; CELL DIFFERENTIATION; FEMALE; FETAL GROWTH RETARDATION; INSULIN RESISTANCE; PLACENTA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SHEEP; TESTOSTERONE;

EID: 84903650425     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-14-0055     Document Type: Article

References (77)

1. Abbott DH, Dumesic DA, Levine JE, Dunaif A & Padmanabhan V 2006 Animal models and fetal programming of PCOS. In Contemporary Endocrinology: Androgen Excess Disorders in Women: Polycystic Ovary Syndrome and Other Disorders, pp 259-272. Eds R Azziz, JE Nestler & D Dewailly. Totowa, NJ: Humana Press, Inc.
2. Abbott DH, Bruns CR, Barnett DK, Dunaif A, Goodfriend TL, Dumesic DA & Tarantal AF 2010 Experimentally induced gestational androgen excess disrupts glucoregulation in rhesus monkey dams and their female offspring. American Journal of Physiology. Endocrinology and Metabolism 299 E741-E751. (doi:10.1152/ajpendo.00058.2010)
3. Abi Salloum B, Veiga-Lopez A, Abbott DH & Padmanabhan V 2012 Developmental programming: gestational exposure to excess testosterone, by its androgenic action, disrupts maternal steroidal and metabolic environment in sheep. 94th Annual Meeting of the Endocrine Society, Houston, TX. Abstract # MON-15 p 145.
4. Alexander G 1964a Studies on the placenta of the sheep (Ovis aries L.). Placental size. Journal of Reproduction and Fertility 7 289-305. (doi:10.1530/jrf.0.0070289)
5. Alexander G 1964b Studies on the placenta of the sheep (Ovis aries L.). Effect of surgical reduction in the number of caruncles. Journal of Reproduction and Fertility 7 307-322. (doi:10.1530/jrf.0.0070307)
6. Ananth CV &Wilcox AJ 2001 Placental abruption and perinatal mortality in the United States. American Journal of Epidemiology 153 332-337. (doi:10.1093/aje/153.4.332) (Pubitemid 32144558)
7. Barker DJ 2004 The developmental origins of adult disease. Journal of the American College of Nutrition 23 588S-595S. (doi:10.1080/07315724.2004. 10719428) (Pubitemid 40096746)
8. Barker DJ 2006 Adult consequences of fetal growth restriction. Clinical Obstetrics and Gynecology 49 270-283. (doi:10.1097/00003081-200606000-00009) (Pubitemid 44317915)
9. Bell AW, Wilkening RB & Meschia G 1987 Some aspects of placental function in chronically heat-stressed ewes. Journal of Developmental Physiology 9 17-29. (Pubitemid 17016201)
10. Bowman CJ, Streck RD & Chapin RE 2010 Maternal-placental insulin-like growth factor (IGF) signaling and its importance to normal embryofetal development. Birth Defects Research. Part B, Developmental and Reproductive Toxicology 89 339-349. (doi:10.1002/bdrb.20249)
11. Carrizo DG, Rastrilla AM, Telleria CM & Aguado LI 1994 Androstenedione stimulates progesterone production in corpora lutea of pregnant rats:an effect not mediated by oestrogen. Journal of Steroid Biochemistry and Molecular Biology 51 191-197. (doi:10.1016/0960-0760(94)90093-0) (Pubitemid 24372863)
12. Crespi EJ, Steckler TL, Mohankumar PS & Padmanabhan V 2006 Prenatal exposure to excess testosterone modifies the developmental trajectory of the insulin-like growth factor system in female sheep. Journal of Physiology 572 119-130. (doi:10.1113/jphysiol.2005.103929)
13. Debus N, Chavatte-Palmer P, Viudes G, Camous S, Rosefort A & Hassoun P 2012 Maternal periconceptional undernutrition in Merinos d'Arles sheep: 1. Effects on pregnancy and reproduction results of dams and offspring growth performances. Theriogenology 77 1453-1465. (doi:10.1016/j.theriogenology.2011. 11.015)
14. Di Renzo GC, Mattei A, Gojnic M & Gerli S 2005 Progesterone and pregnancy. Current Opinion in Obstetrics & Gynecology 17 598-600. (doi:10.1097/01.gco.0000191899.84567.4d) (Pubitemid 41658966)
15. Forbes K & Westwood M 2008 The IGF axis and placental function. a mini review. Hormone Research 69 129-137. (doi:10.1159/000112585) (Pubitemid 351161040)
16. France JT, Mason JI, Magness RR, Murry BA & Rosenfeld CR 1987 Ovine placental aromatase: studies of activity levels, kinetic characteristics and effects of aromatase inhibitors. Journal of Steroid Biochemistry 28 155-160. (doi:10.1016/0022-4731(87)90371-2) (Pubitemid 17130218)
17. Gabory A, Attig L & Junien C 2011 Developmental programming and epigenetics. American Journal of Clinical Nutrition 94 1943S-1952S. (doi:10.3945/ajcn.110.000927)
18. Gardner DS, Ward JW, Giussani DA & Fowden AL 2002 The effect of a reversible period of adverse intrauterine conditions during late gestation on fetal and placental weight and placentome distribution in sheep. Placenta 23 459-466. (doi:10.1053/plac.2002.0830) (Pubitemid 34966029)
19. Gluckman PD, Hanson MA, Cooper C & Thornburg KL 2008 Effect of in utero and early-life conditions on adult health and disease. New England Journal of Medicine 359 61-73. (doi:10.1056/NEJMra0708473) (Pubitemid 351931097)
20. Godfrey KM, Inskip HM & Hanson MA 2011 The long-term effects of prenatal development on growth and metabolism. Seminars in Reproductive Medicine 29 257-265. (doi:10.1055/s-0031-1275518)
21. Gould JB, Madan A, Qin C & Chavez G 2003 Perinatal outcomes in two dissimilar immigrant populations in the United States: a dual epidemiologic paradox. Pediatrics 111 e676-e682. (doi:10.1542/peds.111.6.e676)
22. Grzesiak M, Knapczyκ-Stwora K, Ciereszko RE, Golas A, Wieciech I & Slomczynska M 2014 Androgen deficiency during mid- and late pregnancy alters progesterone production and metabolism in the porcine corpus luteum. Reproductive Sciences 21 778-790. (doi:10.1177/1933719113518991)
23. Handa RJ, Pak TR, Kudwa AE, Lund TD & Hinds L 2008 An alternate pathway for androgen regulation of brain function: activation of estrogen receptor b by the metabolite of dihydrotestosterone, 5a-androstane-3b,17b-diol. Hormones and Behavior 53 741-752. (doi:10.1016/j.yhbeh.2007.09.012)
24. Hartwig IR, Pincus MK, Diemert A, Hecher K & Arck PC 2013 Sex-specific effect of first-trimester maternal progesterone on birthweight. Human Reproduction 28 77-86. (doi:10.1093/humrep/des367)
25. Heasman L, Clarke L, Stephenson TJ & Symonds ME 1999 The influence of maternal nutrient restriction in early to mid-pregnancy on placental and fetal development in sheep. Proceedings of the Nutrition Society 58 283-288. (doi:10.1017/S0029665199000397) (Pubitemid 29398110)
26. HigginsM, Felle P, Mooney EE, Bannigan J & McAuliffe FM 2011 Stereology of the placenta in type 1 and type 2 diabetes. Placenta 32 564-569. (doi:10.1016/j.placenta.2011.04.015)
27. Horie K, Takakura K, Imai K, Liao S & Mori T 1992 Immunohistochemical localization of androgen receptor in the human endometrium, decidua, placenta and pathological conditions of the endometrium. Human Reproduction 7 1461-1466. (Pubitemid 23042175)
28. Jackson LM, Timmer KM & Foster DL 2008 Sexual differentiation of the external genitalia and the timing of puberty in the presence of an antiandrogen in sheep. Endocrinology 149 4200-4208. (doi:10.1210/en.2007-1382)
29. Jindal P, Regan L, Fourkala EO, Rai R, Moore G, Goldin RD & Sebire NJ 2007 Placental pathology of recurrent spontaneous abortion: the role of histopathological examination of products of conception in routine clinical practice: a mini review. Human Reproduction 22 313-316. (doi:10.1093/humrep/ del128) (Pubitemid 46152549)
30. Kaufmann P, Bruns U, Leiser R, Luckhardt M & Winterhager E 1985 The fetal vascularisation of term human placental villi. II. Intermediate and terminal villi. Anatomy and Embryology 173 203-214. (doi:10.1007/BF00316301) (Pubitemid 16182627)
31. Khatri P, Hoffmann B & Schuler G 2013 Androgen receptor is widely expressed in bovine placentomes and up-regulated during differentiation of bovine trophoblast giant cells. Placenta 34 416-423. (doi:10.1016/j.placenta. 2013.01.018)
32. Koong LJ, Garrett WN & Rattray PV 1975 A description of the dynamics of fetal growth in sheep. Journal of Animal Science 41 1065-1068.
33. Leiser R & Kaufmann P 1994 Placental structure: in a comparative aspect. Experimental and Clinical Endocrinology 102 122-134. (doi:10.1055/s-0029-1211275) (Pubitemid 24235550)
34. Leiser R, Kosanke G & Kaufmann P 1991 Human placental vascularization. Structural and quantitative aspects. In Placenta: Basic Research for Clinical Application, pp 32-45. Ed H Soma. Basel: Karger.
35. Leiser R, Krebs C, Ebert B & Dantzer V 1997 Placental vascular corrosion cast studies: a comparison between ruminants and humans. Microscopy Research and Technique 38 76-87. (doi:10.1002/(SICI)1097-0029(19970701/15)38:1/ 2<76::AID-JEMT9>3.0.CO;2-S) (Pubitemid 27328949)
36. Lo JC & Grumbach MM 2001 Pregnancy outcomes in women with congenital virilizing adrenal hyperplasia. Endocrinology and Metabolism Clinics of North America 30 207-229. (doi:10.1016/S0889-8529(08)70027-6) (Pubitemid 32385203)
37. Longtine MS & Nelson DM 2011 Placental dysfunction and fetal programming: the importance of placental size, shape, histopathology, and molecular composition. Seminars in Reproductive Medicine 29 187-196. (doi:10.1055/s-0031-1275515)
38. Louey S, Cock ML & Harding R 2003 Postnatal development of arterial pressure: influence of the intrauterine environment. Archives of Physiology and Biochemistry 111 53-60. (doi:10.1076/apab.111.1.53.15137)
39. Maliqueo M, Lara HE, Sanchez F, Echiburu B, Crisosto N & Sir-Petermann T 2013 Placental steroidogenesis in pregnant women with polycystic ovary syndrome. European Journal of Obstetrics, Gynecology, and Reproductive Biology 166 151-155. (doi:10.1016/j.ejogrb.2012.10.015)
40. Manikkam M, Crespi EJ, Doop DD, Herkimer C, Lee JS, Yu S, Brown MB, Foster DL & Padmanabhan V 2004 Fetal programming: prenatal testosterone excess leads to fetal growth retardation and postnatal catch-up growth in sheep. Endocrinology 145 790-798. (doi:10.1210/en.2003-0478) (Pubitemid 38183822)
41. Martyniuk CJ & Denslow ND 2012 Exploring androgen-regulated pathways in teleost fish using transcriptomics and proteomics. Integrative and Comparative Biology 52 695-704. (doi:10.1093/icb/ics072)
42. McDonald EA & Wolfe MW 2009 Adiponectin attenuation of endocrine function within human term trophoblast cells. Endocrinology 150 4358-4365. (doi:10.1210/en.2009-0058)
43. Misra DP, Salafia CM, Miller RK & Charles AK 2009 Non-linear and gender-specific relationships among placental growth measures and the fetoplacental weight ratio. Placenta 30 1052-1057. (doi:10.1016/j.placenta.2009. 09.008)
44. Morrison JL 2008 Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clinical and Experimental Pharmacology & Physiology 35 730-743. (doi:10.1111/j.1440-1681.2008.04975.x) (Pubitemid 351725247)
45. Mossman HW 1987 Vertebrate Fetal Membranes: Comparative Ontogeny and Morphology; Evolution; Phylogenetic Significance; Basic Functions; Research Opportunities. London: Macmillan Press Ltd. Nestler JE 1993 Regulation of the aromatase activity of human placental cytotrophoblasts by insulin, insulin-like growth factor-I, and -II. Journal of Steroid Biochemistry and Molecular Biology 44 449-457. (doi:10.1016/0960-0760(93)90249-V)
46. Nijland MJ, Ford SP & Nathanielsz PW 2008 Prenatal origins of adult disease. Current Opinion in Obstetrics & Gynecology 20 132-138. (doi:10.1097/GCO.0b013e3282f76753) (Pubitemid 351498764)
47. NRC Committee on the Nutrient Requirements of Small Ruminant 2007 Nutrient Requirements of Small Ruminants. Sheep, Goats, Cervids, and New World Camelids. Washington, DC: The National Academies Press.
48. Osgerby JC, Gadd TS &Wathes DC 2003 Effect of maternal body condition on placental and fetal growth and the insulin-like growth factor axis in Dorset ewes. Reproduction 125 717-731. (doi:10.1530/rep.0.1250717) (Pubitemid 36622179)
49. Otto-Duessel M, He M & Jones JO 2012 Tissue-selective regulation of androgen-responsive genes. Endocrine Research 37 203-215. (doi:10.3109/07435800. 2012.668254)
50. Padmanabhan V & Veiga-Lopez A 2011 Developmental origin of reproductive and metabolic dysfunctions: androgenic versus estrogenic reprogramming. Seminars in Reproductive Medicine 29 173-186. (doi:10.1055/s-0031-1275519)
51. Padmanabhan V & Veiga-Lopez A 2013 Sheep models of polycystic ovary syndrome phenotype. Molecular and Cellular Endocrinology 373 8-20. (doi:10.1016/j.mce.2012.10.005)
52. Padmanabhan V, Sarma HN, Savabieasfahani M, Steckler TL & Veiga-Lopez A 2010 Developmental reprogramming of reproductive and metabolic dysfunction in sheep: native steroids vs. environmental steroid receptor modulators. International Journal of Andrology 33 394-404. (doi:10.1111/j.1365-2605.2009. 01024.x)
53. Palomba S, Russo T, Falbo A, Di Cello A, Tolino A, Tucci L, La Sala GB & Zullo F 2013 Macroscopic and microscopic findings of the placenta in women with polycystic ovary syndrome. Human Reproduction 28 2838-2847. (doi:10.1093/humrep/det250)
54. Parker VJ & Douglas AJ 2010 Stress in early pregnancy: maternal neuroendocrine-immune responses and effects. Journal of Reproductive Immunology 85 86-92. (doi:10.1016/j.jri.2009.10.011)
55. Penninga L & Longo LD 1998 Ovine placentome morphology: effect of high altitude, long-term hypoxia. Placenta 19 187-193. (doi:10.1016/S0143- 4004(98)90008-X) (Pubitemid 28112203)
56. Phillips DI, Jones A & Goulden PA 2006 Birth weight, stress, and the metabolic syndrome in adult life. Annals of the New York Academy of Sciences 1083 28-36. (doi:10.1196/annals.1367.027) (Pubitemid 44955465)
57. Qin JZ, Pang LH, Li MJ, Fan XJ, Huang RD & Chen HY 2013 Obstetric complications in women with polycystic ovary syndrome: a systematic review and meta-analysis. Reproductive Biology and Endocrinology 11 56. (doi:10.1186/1477-7827-11-56)
58. Recabarren SE, Rojas-Garcia PP, Recabarren MP, Alfaro VH, Smith R, Padmanabhan V & Sir-Petermann T 2008 Prenatal testosterone excess reduces sperm count and motility. Endocrinology 149 6444-6448. (doi:10.1210/en.2008- 0785)
59. Rees S, Mallard C, Breen S, Stringer M, Cock M & Harding R 1998 Fetal brain injury following prolonged hypoxemia and placental insufficiency: a review. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 119 653-660. (doi:10.1016/S1095-6433(98)01001-0) (Pubitemid 28219064)
60. Regnault TR, Galan HL, Parker TA & Anthony RV 2002 Placental development in normal and compromised pregnancies - a review. Placenta 23 S119-S129. (doi:10.1053/plac.2002.0792) (Pubitemid 39658622)
61. Reik W, Constancia M, Fowden A, Anderson N, Dean W, Ferguson-Smith A, Tycko B & Sibley C 2003 Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. Journal of Physiology 547 35-44. (doi:10.1113/jphysiol.2002.033274) (Pubitemid 36285159)
62. Roberts CT, Owens JA & Sferruzzi-Perri AN 2008 Distinct actions of insulin-like growth factors (IGFs) on placental development and fetal growth: lessons from mice and guinea pigs. Placenta 29 (Suppl A) S42-S47. (doi:10.1016/j.placenta.2007.12.002)
63. Rossi R, Scillitani G, Vimercati A, Fiore MG, Mastrodonato M & Resta L 2012 Diabetic placenta: ultrastructure and morphometry of the term villi. Analytical and Quantitative Cytology and Histology 34 239-247.
64. Simmons RA 2009 Developmental origins of adult disease. Pediatric Clinics of North America 56 449-466. (doi:10.1016/j.pcl.2009.03.004)
65. Sir-Petermann T, Maliqueo M, Angel B, Lara HE, Perez-Bravo F & Recabarren SE 2002 Maternal serum androgens in pregnant women with polycystic ovarian syndrome: possible implications in prenatal androgenization. Human Reproduction 17 2573-2579. (doi:10.1093/humrep/17.10.2573) (Pubitemid 35174106)
66. Sir-Petermann T, Ladron de Guevara A, Villarroel AC, Preisler J, Echiburu B & Recabarren S 2012 Polycystic ovary syndrome and pregnancy. Revista Médica de Chile 140 919-925. (doi:10.4067/S0034-98872012000700015)
67. Steckler T, Wang J, Bartol FF, Roy SK & Padmanabhan V 2005 Fetal programming: prenatal testosterone treatment causes intrauterine growth retardation, reduces ovarian reserve and increases ovarian follicular recruitment. Endocrinology 146 3185-3193. (doi:10.1210/en.2004-1444) (Pubitemid 41007051)
68. Steckler T, Manikkam M, Inskeep EK & Padmanabhan V 2007 Developmental programming: follicular persistence in prenatal testosteronetreated sheep is not programmed by androgenic actions of testosterone. Endocrinology 148 3532-3540. (doi:10.1210/en.2007-0339) (Pubitemid 46997017)
69. Symonds ME, Heasman L, Clarke L, Firth K & Stephenson T 1998 Maternal nutrition and disproportionate placental-to-fetal growth. Biochemical Society Transactions 26 91-96. (Pubitemid 28263674)
70. Szekeres-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T & Szereday L 2001 Progesterone as an immunomodulatory molecule. International Immunopharmacology 1 1037-1048. (doi:10.1016/S1567-5769(01)00035-2) (Pubitemid 32434423)
71. Uzelac PS, Li X, Lin J, Neese LD, Lin L, Nakajima ST, Bohler H & Lei Z 2010 Dysregulation of leptin and testosterone production and their receptor expression in the human placenta with gestational diabetes mellitus. Placenta 31 581-588. (doi:10.1016/j.placenta.2010.04.002)
72. Vatnick I, Ignotz G, McBride BW & Bell AW 1991 Effect of heat stress on ovine placental growth in early pregnancy. Journal of Developmental Physiology 16 163-166.
73. Veiga-Lopez A, Lee JS & Padmanabhan V 2010 Developmental programming: insulin sensitizer treatment improves reproductive function in prenatal testosterone-treated female sheep. Endocrinology 151 4007-4017. (doi:10.1210/en.2010-0124)
74. Veiga-Lopez A, Steckler TL, Abbott DH, Welch KB, MohanKumar PS, Phillips DJ, Refsal K & Padmanabhan V 2011 Developmental programming: impact of excess prenatal testosterone on intrauterine fetal endocrine milieu and growth in sheep. Biology of Reproduction 84 87-96. (doi:10.1095/biolreprod.110.086686)
75. Vonnahme KA, Hess BW, Nijland MJ, Nathanielsz PW & Ford SP 2006 Placentomal differentiation may compensate for maternal nutrient restriction in ewes adapted to harsh range conditions. Journal of Animal Science 84 3451-3459. (doi:10.2527/jas.2006-132) (Pubitemid 44862361)
76. Wallace JM, Aitken RP, Cheyne MA & Humblot P 1997 Pregnancy-specific protein B and progesterone concentrations in relation to nutritional regimen, placental mass and pregnancy outcome in growing adolescent ewes carrying singleton fetuses. Journal of Reproduction and Fertility 109 53-58. (doi:10.1530/jrf.0.1090053)
77. Wallace JM, Bourke DA, Aitken RP, Palmer RM, Da Silva P & Cruickshank MA 2000 Relationship between nutritionally-mediated placental growth restriction and fetal growth, body composition and endocrine status during late gestation in adolescent sheep. Placenta 21 100-108. (doi:10.1053/plac.1999.0440) (Pubitemid 30099501)