Prenatal androgens affect development and behavior in primates

Building Babies: Primate Development in Proximate and Ultimate Perspective

Volumn , Issue , 2013, Pages 103-131

  Smith, A S ^a   Birnie, A K ^b   French, J A ^b  

^a FLORIDA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA AT OMAHA   (United States)

Author keywords

Infant outcomes; Prenatal exposure; Sex differentiation; Testosterone; Uterine environment

Indexed keywords

EID: 84872528299     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-4060-4_5     Document Type: Chapter

References (210)

1. Abbott DH (1984) Differentiation of sexual behaviour in female marmoset monkeys: effects of neonatal testosterone or a male co-twin. Prog Brain Res 61:349-358
2. Abbott DH, Bird I (2009) Nonhuman primates as models for human adrenal androgen production: function and dysfunction. Rev Endocr Metab Disord 10:33-42
3. Abbott DH, Hearn JP (1978a) Physical, hormonal and behavioural aspects of sexual development in the marmoset monkey, Callithrix jacchus. J Reprod Fertil 53:155-166
4. Abbott DH, Hearn JP (1978b) The effects of neonatal exposure to testosterone on the development of behaviour in female marmoset monkeys. Ciba Found Symp 62:299-327
5. Abbott DH, Dumesic DA, Eisner JR, Colman RJ, Kemnitz JW (1998) Insights into the development of polycystic ovary syndrome (PCOS) from studies of prenatally androgenized female rhesus monkeys. Trends Endocrinol Metab 9:62-67
6. Abbott DH, Barnett DK, Bruns CM, Dumesic DA (2005) Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome? Hum Reprod Update 11:357-374
7. Abbott DH, Barnett DK, Levine JE, Padmanabhan V, Dumesic DA, Jacoris S, Tarantal AF (2008) Endocrine antecedents of polycystic ovary syndrome (PCOS) in fetal and infant prenatally androgenized female rhesus monkeys. Biol Reprod 79:154-163
8. Abbott DH, Tarantal AF, Dumesic DA (2009) Fetal, infant, adolescent and adult phenotypes of polycystic ovary syndrome in prenatally androgenized female rhesus monkeys. Am J Primatol 71:776-784
9. 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. Am J Physiol Endocrinol Metab 299:E741-E751
10. Ahmed SF, Cheng A, Dovey L, Hawkins JR, Martin H, Rowland J, Shimura N, Tait AD, Hughes IA (2000) Phenotypic features, androgen receptor binding, and mutational analysis in 278 clinical cases reported as androgen insensitivity syndrome. J Clin Endocrinol Metab 85:658-665
11. Albrecht ED, Pepe GJ (1990) Placental steroid hormone biosynthesis in primate pregnancy. Endocr Rev 11:124-150
12. Alexander GM, Hines M (2002) Sex differences in response to children's toys in nonhuman primates (Cercopithecus aethiops sabaeus). Evol Hum Behav 23:467-479
13. Alexander G, Wilcox T, Woods R (2009) Sex differences in infants' visual interest in toys. Arch Sex Behav 38:427-433
14. Altmann J, Lynch JW, Nguyen N, Alberts SC, Gesquiere LR (2004) Life-history correlates of steroid concentrations in wild peripartum baboons. Am J Primatol 64:95-106
15. Anderson H, Fogel N, Grebe SK, Singh RJ, Taylor RL, Dunaif A (2010) Infants of women with polycystic ovary syndrome have lower cord blood androstenedione and estradiol levels. J Clin Endocrinol Metab 95:2180-2186
16. Andrade MCR, Ribeiro CT, Silva VF, Molinaro EM, Gonçalves MÂB, Marques MAP, Cabello PH, Leite JPG (2004) Biologic data of Macaca mulatta, Macaca fascicularis and Saimiri sciureus used for research at the Fiocruz primate center. Mem Inst Oswaldo Cruz 99:581-589
17. Arnold AP (2009) The organizational-activational hypothesis as the foundation for a uni fied theory of sexual differentiation of all mammalian tissues. Horm Behav 55:570-578
18. Arnold AP, Xu J, Grisham W, Chen X, Kim YH, Itoh Y (2004) Minireview: sex chromosomes and brain sexual differentiation. Endocrinology 145:1057-1062
19. Atkinson G, Campbell DJ, Cawood ML, Oakey RE (1996) Steroids in human intrauterine fluids of early pregnancy. Clin Endocrinol 44:435-440
20. Aujard F, Perret M (1998) Age-related effects on reproductive function and sexual competition in the male prosimian primate, Microcebus murinus. Physiol Behav 64:513-519
21. Auyeung B, Baron-Cohen S, Ashwin E, Knickmeyer R, Taylor K, Hackett G, Hines M (2009) Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys. Psychol Sci 20:144-148
22. Bammann BL, Coulam CB, Jiang NS (1980) Total and free testosterone during pregnancy. Am J Obstet Gynecol 137:293-298
23. Bao A-M, Swaab DF (2010) Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 16:550-565
24. Barker DJP (1998) Programming the baby. In: Barker DJP (ed) Mothers, babies and health in later life. Churchill Livingstone, Edinburgh, pp 13-42
25. Barry JA, Kay AR, Navaratnarajah R, Iqbal S, Bamfo JEAK, David AL, Hines M, Hardiman PJ (2010) Umbilical vein testosterone in female infants born to mothers with polycystic ovary syndrome is elevated to male levels. J Obstet Gynaecol 30:444-446
26. Batty KA, Herbert J, Keverne EB, Vellucci SV (1986) Differences in blood levels of androgens in female talapoin monkeys related to their social status. Neuroendocrinology 44:347-354
27. Bendsen E, Byskov AG, Laursen SB, Larsen HP, Andersen CY, Westergaard LG (2003) Number of germ cells and somatic cells in human fetal testes during the first weeks after sex differentiation. Hum Reprod 18:13-18
28. Berenbaum SA (1999) Effects of early androgens on sex-typed activities and interests in adolescents with congenital adrenal hyperplasia. Horm Behav 35:102-110
29. Berenbaum SA, Bailey JM (2003) Effects on gender identity of prenatal androgens and genital appearance: evidence from girls with congenital adrenal hyperplasia. J Clin Endocrinol Metab 88:1102-1106
30. Berenbaum SA, Hines M (1992) Early androgens are related to childhood sex-typed toy preferences. Psychol Sci 3:203-206
31. Birnie AK, Smith AS, Nali C, French JA (2011) Social and developmental in fluences on urinary androgen levels in young male white-faced marmosets (Callithrix geoffroyi). Am J Primatol 73:378-385
32. Birnie AK, Hendricks SE, Smith AS, Milam R, French JA (in press) Maternal gestational androgens are associated with decreased juvenile play in white-faced marmosets (Callithrix geoffroyi) Horm Behav Boehmer AL, Brinkmann AO, Sandkuijl LA, Halley DJ, Niermeijer MF, Andersson S, de Jong FH, Kayserili H, de Vroede MA, Otten BJ, Rouwe CW, Mendonca BB, Rodrigues C, Bode HH, de Ruiter PE, Delemarre-van de Waal HA, Drop SL (1999) 17Beta-hydroxysteroid dehydrogenase-3 de ficiency: diagnosis, phenotypic variability, population genetics, and worldwide distribution of ancient and de novo mutations. J Clin Endocrinol Metab 84:4713-4721
33. Bogardus C, Lillioja S, Mott DM, Hollenbeck C, Reaven G (1985)Relationship between degree of obesity and in vivo insulin action in man. Am J Physiol Endocrinol Metab 248:E286-E291
34. Boomsma CM, Eijkemans MJC, Hughes EG, Visser GHA, Fauser BCJM, Macklon NS (2006) A meta-analysis of pregnancy outcomes in women with polycystic ovary syndrome. Hum Reprod Update 12:673-683
35. Braga LH, Pippi Salle JL (2009) Congenital adrenal hyperplasia: a critical appraisal of the evolution of feminizing genitoplasty and the controversies surrounding gender reassignment. Eur J Pediatr Surg 19:203-210
36. Brown GR, Nevison CM, Fraser HM, Dixson AF (1999) Manipulation of postnatal testosterone levels affects phallic and clitoral development in infant rhesus monkeys. Int J Androl 22:119-128
37. Bruns CM, Baum ST, Colman RJ, Eisner JR, Kemnitz JW, Weindruch R, Abbott DH (2004) Insulin resistance and impaired insulin secretion in prenatally androgenized male rhesus monkeys. J Clin Endocrinol Metab 89:6218-6223
38. Burger HG (2002) Androgen production in women. Fertil Steril 77:3-5
39. Caine N, Mitchell G (1979) A review of play in the genus Macaca: social correlates. Primates 20:535-546
40. Capel B, Coveney D (2004) Frank Lillie's freemartin: illuminating the pathway to 21st century reproductive endocrinology. J Exp Zool A Comp Exp Biol 301:853-856
41. Carlsen SM, Jacobsen G, Romundstad P (2006) Maternal testosterone levels during pregnancy are associated with offspring size at birth. Eur J Endocrinol 155:365-370
42. Caro JF, Dohm LG, Pories WJ, Sinha MK (1989) Cellular alterations in liver, skeletal muscle, and adipose tissue responsible for insulin resistance in obesity and type II diabetes. Diabetes Metab Rev 5:665-689
43. Castracane VD, Asch RH (1995) Testosterone and androstenedione in premature ovarian failure pregnancies: evidence for an ovarian source of androgens in early pregnancy. Hum Reprod 10:677-680
44. Castracane VD, Goldzieher JW (1983) Plasma androgens during early pregnancy in the baboon (Papio cynocephalus). Fertil Steril 39:553-559
45. Castracane V, Stewart D, Gimpel T, Overstreet J, Lasley B (1998) Maternal serum androgens in human pregnancy: early increases within the cycle of conception. Hum Reprod 13:460-464
46. Challis JRG, Davies IJ, Benirschke K, Hendrickx AG, Ryan KJ (1975) The effects of dexamethasone on the peripheral plasma concentrations of androstenedione, testosterone and cortisol in the pregnant rhesus monkey. Endocrinology 96:185-192
47. Chambers PL, Hearn JP (1979) Peripheral plasma levels of progesterone, oestradiol-17 beta, oestrone, testosterone, androstenedione and chorionic gonadotrophin during pregnancy in the marmoset monkey. J Reprod Fertil 56:23-32
48. Clark AS, Goldman-Rakic PS (1989) Gonadal hormones in fluence the emergence of cortical function in nonhuman primates. Behav Neurosci 103:1287-1295
49. Clark AS, MacLusky NJ, Goldman-Rakic PS (1988) Androgen binding and metabolism in the cerebral cortex of the developing rhesus monkey. Endocrinology 123:932-940
50. Cloke B, Huhtinen K, Fusi L, Kajihara T, Yliheikkila M, Ho K-K, Teklenburg G, Lavery S, Jones MC, Trew G, Kim JJ, Lam EWF, Cartwright JE, Poutanen M, Brosens JJ (2008) The androgen and progesterone receptors regulate distinct gene networks and cellular functions in decidualizing endometrium. Endocrinology 149:4462-4474
51. Cohen-Bendahan CCC, van de Beek C, Berenbaum SA (2005) Prenatal sex hormone effects on child and adult sex-typed behavior: methods and findings. Neurosci Biobehav Rev 29:353-384
52. Cole B, Hensinger K, Maciel GA, Chang RJ, Erickson GF (2006) Human fetal ovary development involves the spatiotemporal expression of p450c17 protein. J Clin Endocrinol Metab 91:3654-3661
53. Conley AJ, Pattison JC, Bird IM (2004)Variations in adrenal androgen production among (nonhuman) primates. Semin Reprod Med 22:311, 326
54. Coviello AD, Legro RS, Dunaif A (2006) Adolescent girls with polycystic ovary syndrome have an increased risk of the metabolic syndrome associated with increasing androgen levels independent of obesity and insulin resistance. J Clin Endocrinol Metab 91:492-497
55. d'Aux RCD, Murphy BEP (1974) Androgens in the human fetus. J Steroid Biochem Mol Biol 5:207-210
56. de Vries MJ, Dekker GA, Schoemaker J (1998) Higher risk of preeclampsia in the polycystic ovary syndrome: a case control study. Eur J Obstet Gynecol Reprod Biol 76:91-95
57. DeFronzo R (1992) Pathogenesis of Type 2 (non-insulin dependent) diabetes mellitus: a balanced overview. Diabetologia 35:389-397
58. Dixson AF (1986) Plasma testosterone concentrations during postnatal development in the male common marmoset. Folia Primatol 47:166-170
59. Dixson AF (1993) Callitrichid mating systems: laboratory and field approaches to studies of monogamy and polyandry. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford University Press, New York, pp 164-175
60. Dumesic DA, Abbott DH, Eisner JR, Goy RW (1997) Prenatal exposure of female rhesus monkeys to testosterone propionate increases serum luteinizing hormone levels in adulthood. Fertil Steril 67:155-163
61. Dunaif A (1992) Polycystic ovary syndrome and obesity. In: Bjorntorp P, Brodoff BN (eds) Obesity. J.B. Lippincott Co, Philadelphia, pp 594-605
62. Dunaif A, Graf M, Mandeli J, Laumas V, Dobrjansky A (1987) Characterization of groups of hyperandrogenic women with acanthosis nigricans, impaired glucose tolerance, and/or hyperinsulinemia. J Clin Endocrinol Metab 65:499-507
63. Dunaif A, Segal KR, Shelley DR, Green G, Dobrjansky A, Licholai T (1992) Evidence for distinctive and intrinsic defects in insulin action in polycystic ovary syndrome. Diabetes 41:1257-1266
64. Eaton GG, Goy RW, Phoenix CH (1973) Effects of testosterone treatment in adulthood on sexual behaviour of female pseudohermaphrodite rhesus monkeys. Nat New Biol 242:119-120
65. Eaton GG, Worlein JM, Glick BB (1990) Sex differences in Japanese macaques (Macaca fuscata): effects of prenatal testosterone on juvenile social behavior. Horm Behav 24:270-283
66. Ehrhardt AA, Meyer-Bahlburg HF (1981) Effects of prenatal sex hormones on gender-related behavior. Science 211:1312-1318
67. Ehrmann DA (2005) Polycystic ovary syndrome. N Engl J Med 352:1223-1236
68. Ehrmann DA, Liljenquist DR, Kasza K, Azziz R, Legro RS, Ghazzi MN, PCOS/Troglitazone Study Group (2006) Prevalence and predictors of the metabolic syndrome in women with polycystic ovary syndrome. J Clin Endocrinol Metab 91:48-53
69. Eisner JR, Dumesic DA, Kemnitz JW, Abbott DH (2000) Timing of prenatal androgen excess determines differential impairment in insulin secretion and action in adult female rhesus monkeys. J Clin Endocrinol Metab 85:1206-1210
70. Eisner JR, Barnett MA, Dumesic DA, Abbott DH (2002) Ovarian hyperandrogenism in adult female rhesus monkeys exposed to prenatal androgen excess. Fertil Steril 77:167-172
71. Eisner JR, Dumesic DA, Kemnitz JW, Colman RJ, Abbott DH (2003) Increased adiposity in female rhesus monkeys exposed to androgen excess during early gestation. Obes Res 11:279-286
72. Ellinwood WE, Baughman WL, Resko JA (1982) The effects of gonadectomy and testosterone treatment on luteinizing hormone secretion in fetal rhesus monkeys. Endocrinology 110:183-189
73. Ellinwood WE, Stanczyk FZ, Lazur JJ, Novy MJ (1989) Dynamics of steroid biosynthesis during the luteal-placental shift in rhesus monkeys. J Clin Endocrinol Metab 69:348-355
74. Finegan JA, Bartleman B, Wong PY (1989) A window for the study of prenatal sex hormone in fluences on postnatal development. J Genet Psychol 150:101-112
75. Fite JE, French JA, Patera KJ, Hopkins EC, Rukstalis M, Ross CN (2005) Elevated urinary testosterone excretion and decreased maternal caregiving effort in marmosets when conception occurs during the period of infant dependence. Horm Behav 47:39-48
76. Ford SM (1994) Evolution of sexual dimorphism in body weight in platyrrhines. Am J Primatol 34:221-244
77. Forest MG (1983) Role of androgens in fetal and pubertal development. Horm Res 18:69-83
78. Fowler PA, Anderson RA, Saunders PT, Kinnell H, Mason JI, Evans DB, Bhattacharya S, Flannigan S, Franks S, Monteiro A, O'Shaughnessy PJ (2011) Development of steroid signaling pathways during primordial follicle formation in the human fetal ovary. J Clin Endocrinol Metab 96:1754-1762
79. French JA, Smith AS, Birnie AK (2010) Maternal gestational androgen levels in female marmosets (Callithrix geoffroyi) vary across trimesters but do not vary with the sex ratio of litters. Gen Comp Endocrinol 165:309-314
80. Gant NF, Hutchinson HT, Siiteri PK, MacDonald PC (1971) Study of the metabolic clearance rate of dehydroisoandrosterone sulfate in pregnancy. Am J Obstet Gynecol 15:555-563
81. Gemer O, Sevillia J, Zalis J, Segal S (1997) Umbilical cord androgens in infants of diabetic mothers. Arch Gynecol Obstet 259:139-141
82. George MM, New MI, Ten S, Sultan C, Bhangoo A (2010) The clinical and molecular heterogeneity of 17 b HSD-3 enzyme de ficiency. Horm Res Paediatr 74:229-240
83. Gibber JR, Goy RW (1985) Infant-directed behavior in young rhesus monkeys: sex differences and effects of prenatal androgens. Am J Primatol 8:225-237
84. Ginther AJ, Carlson AA, Ziegler TE, Snowdon CT (2002) Neonatal and pubertal development in males of a cooperatively breeding primate, the cotton-top tamarin (Saguinus oedipus oedipus). Biol Reprod 66:282-290
85. Gitau R, Adams D, Fisk NM, Glover V (2005)Fetal plasma testosterone correlates positively with cortisol. Arch Dis Child Fetal Neonatal Ed 90:F166-F169
86. Glass AR, Klein T (1981) Changes in maternal serum total and free androgen levels in early pregnancy: lack of correlation with fetal sex. Am J Obstet Gynecol 140:656-660
87. Goldschmidt B, Moraes IA, Souza LM, Paulino FS, Pissinatti A, Mársico FF, Ferreira AMR, Pinho TG (2005) Occurrence of virilization signals in a female marmoset Leontopithecus chrysomelas (Callitrichidae; Primates) with 46, XX/46, XY chimerism. Isr J Vet Med 60:86-88
88. Goldzieher JW, Green JA (1962) The polycystic ovary. I. Clinical and histologic features. J Clin Endocrinol Metab 22:325-338
89. Goy RW (1981) Differentiation of male social traits in female rhesus macaques by prenatal treatment with androgens: variation in type of androgen, duration, and timing of treatment. In: Resko JA (ed) Fetal endocrinology. Academic, New York, pp 319-339
90. Goy RW (1996) Patterns of juvenile behavior following early hormonal interventions. In: Magnusson D (ed) The lifespan development of individuals: behavioral, neurobiological, and psychosocial perspectives. Cambridge University Press, New York, pp 296-314
91. Goy RW, McEwen BS (1980)Sexual differentiation of the brain. MIT Press, Cambridge, 236 pp
92. Goy RW, Resko JA (1972) Gonadal hormones and behavior of normal and pseudohermaphroditic nonhuman female primates. Recent Prog Horm Res 28:707-733
93. Goy RW, Robinson JA (1982) Prenatal exposure of rhesus monkeys to patent androgens: morphological, behavioral, and physiological consequences. In: Hunt VR, Smith MK, Worth D (eds) Banbury report II: environmental factors in human growth and development. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 355-378
94. Goy RW, Bercovitch FB, McBrair MC (1988a) Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Horm Behav 22:552-571
95. Goy RW, Uno H, Sholl SA (1988b) Psychological and anatomical consequences of prenatal exposure to androgens in female rhesus. In: Mori T, Nagasawa H (eds) Toxicity of hormones in prenatal life. CRC, Boca Raton, pp 127-142
96. Guard HJ, Newman JD, Roberts RL (2002) Morphine administration selectively facilitates social play in common marmosets. Dev Psychobiol 41:37-49
97. Hassett JM, Siebert ER, Wallen K (2008) Sex differences in rhesus monkey toy preferences parallel those of children. Horm Behav 54:359-364
98. Herman RA, Jones B, Mann DR, Wallen K (2000) Timing of prenatal androgen exposure: anatomical and endocrine effects on juvenile male and female rhesus monkeys. Horm Behav 38:52-66
99. Herman RA, Zehr JL, Wallen K (2006) Prenatal androgen blockade accelerates pubertal development in male rhesus monkeys. Psychoneuroendocrinology 31:118-130
100. Hines M (2004)Brain gender. Oxford University Press, New York, 336 pp
101. Hines M, Kaufman FR (1994) Androgen and the development of human sex-typical behavior: rough-and-tumble play and sex of preferred playmates in children with congenital adrenal hyperplasia (CAH). Child Dev 65:1042-1053
102. Hines M, Golombok S, Rust J, Johnston KJ, Golding J, Avon Longitudinal Study of Parents and Children Study Team (2002) Testosterone during pregnancy and gender role behavior of preschool children: a longitudinal, population study. Child Dev 73:1678-1687
103. Hiort O (2002) Androgens and puberty. Best Pract Res Clin Endocrinol Metab 16:31-41
104. Hoar RM, Monie IW (1981) Comparative development of speci fic organ systems. In: Kimmel CA, Buelke-Sam J (eds) Developmental toxicology. Raven, New York, pp 13-33
105. Hodges JK, Tarara R, Wangula C (1984) Circulating steroids and the relationship between ovarian and placental secretion during early and mid pregnancy in the baboon. Am J Primatol 7:357-366
106. Hönekopp J, Thierfelder C (2009) Relationships between digit ratio (2D:4D) and sex-typed play behavior in pre-school children. Pers Individ Dif 47:706-710
107. Huhtaniemi I (1994) Fetal testis - a very special endocrine organ. Eur J Endocrinol 130:25-31
108. Ibanez L, Potau N, Francois I, de Zegher F (1998) Precocious pubarche, hyperinsulinism, and ovarian hyperandrogenism in girls: relation to reduced fetal growth. J Clin Endocrinol Metab 83:3558-3562
109. Isachenko EF, Nayudu PL, Isachenko VV, Nawroth F, Michelmann HW (2002) Congenitally caused fused labia in the common marmoset (Callithrix jacchus). J Med Primatol 31:350-355
110. Jones HW Jr, Verkauf BS (1971) Congenital adrenal hyperplasia: age at menarche and related events in puberty. Am J Obstet Gynecol 15:292-298
111. Kaplan HS, Gangestad SW (2005) Life history theory and evolutionary psychology. In: Buss DM (ed) The handbook of evolutionary psychology. Wiley, Hoboken, pp 68-95
112. Kasckow JW, Aguilera G, Mulchahey JJ, Sheriff S, Herman JP (2003) In vitro regulation of corticotropin-releasing hormone. Life Sci 73:769-781
113. Kemnitz JW, Sladky KK, Flitsch TJ, Pomerantz SM, Goy RW (1988)Androgenic in fluences on body size and composition of adult rhesus monkeys. Am J Physiol Endocrinol Metab 255:E857-E864
114. Kissebah AH, Peiris AN (1989) Biology of regional body fat distribution: relationship to noninsulin-dependent diabetes mellitus. Diabetes Metab Rev 5:83-109
115. Knickmeyer R, Baron-Cohen S, Wheelwright S (2005) Gender-typed play and amniotic testosterone. Dev Psychol 41:517-528
116. Kousta E, Papathanasiou A, Skordis N (2010) Sex determination and disorders of sex development according to the revised nomenclature and classi fication in 46, XX individuals. Hormones 9:218-231
117. Licht P, Hayes T, Tsai P, Cunha G, Kim H, Golbus M, Hayward S, Martin MC, Jaffe RB, Glickman SE (1998) Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 1. Urogenital morphology and placental androgen production during fetal life. J Reprod Fertil 113:105-116
118. Lillie FR (1917) Sex-determination and sex-differentiation in mammals. Proc Natl Acad Sci USA 3:464-470
119. Linn S, Lieberman E, Schoenbaum SC, Monson RR, Stubblefield PG, Ryan KJ (1988) Adverse outcomes of pregnancy in women exposed to diethylstilbestrol in utero. J Reprod Med 33:3-7
120. Lovejoy J, Wallen K (1988) Sexually dimorphic behavior in group-housed rhesus-monkeys (Macaca mulatta) at 1 year of age. Psychobiology 16:348-356
121. Mann DR, Akinbami MA, Gould KG, Paul K, Wallen K (1998) Sexual maturation in male rhesus monkeys: importance of neonatal testosterone exposure and social rank. J Endocrinol 156:493-501
122. Mapes S, Tarantal AF, Parker CR, Moran FM, Bahr JM, Pyter L, Conley AJ (2002) Adrenocortical cytochrome b5 expression during fetal development of the rhesus macaque. Endocrinology 143:1451-1458
123. Marson J, Meuris S, Cooper RW, Jounannet P (1991) Puberty in the male chimpanzee: time-related variations in luteinizing hormone, follicle-stimulating hormone, and testosterone. Biol Reprod 44:456-460
124. Martin DE, Swenson RB, Collins DC (1977) Correlation of serum testosterone levels with age in male chimpanzees. Steroids 29:471-481
125. McEwen BS (1981) Neural gonadal steroid actions. Science 211:1303-1311
126. McNulty WP, Novy MJ, Walsh SW (1981) Fetal and postnatal development of the adrenal glands in Macaca mulatta. Biol Reprod 25:1079-1089
127. Merke DP, Bornstein SR (2005) Congenital adrenal hyperplasia. Lancet 365:2125-2136
128. Mesiano S, Jaffe RB (1997) Developmental and functional biology of the primate fetal adrenal cortex. Endocr Rev 18:378-403
129. Meulenberg PMM, Hofman JA (1991) Maternal testosterone and fetal sex. J Steroid Biochem Mol Biol 39:51-54
130. Milewich L, Gomez-Sanchez C, Madden JD, Bradfield DJ, Parker PM, Smith SL, Carr BR, Edman CD, MacDonald PC (1978) Dehydroisoandrosterone sulfate in peripheral blood of premenopausal, pregnant and postmenopausal women and men. J Steroid Biochem Mol Biol 9:1159-1164
131. Morales AJ, Laughlin GA, Butzow T, Maheshwari H, Baumann G, Yen SS (1996) Insulin, somatotropic, and luteinizing hormone axes in lean and obese women with polycystic ovary syndrome: common and distinct features. J Clin Endocrinol Metab 81:2854-2864
132. Morris JA, Jordan CL, Breedlove SM (2004) Sexual differentiation of the vertebrate nervous system. Nat Neurosci 7:1034-1039
133. Murphy VE, Smith R, Giles WB, Clifton VL (2006) Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocr Rev 27:141-169
134. Nagamani M, McDonough PG, Ellegood JO, Mahesh VB (1979) Maternal and amniotic fluid steroids throughout human pregnancy. Am J Obstet Gynecol 15:674-680
135. Nimkarn S, New MI (2010) Congenital adrenal hyperplasia due to 21-hydroxylase de ficiency: a paradigm for prenatal diagnosis and treatment. Ann N Y Acad Sci 1192:5-11
136. Nordenström A, Servin A, Bohlin G, Larsson A, Wedell A (2002) Sex-typed toy play behavior correlates with the degree of prenatal androgen exposure assessed by CYP21 genotype in girls with congenital adrenal hyperplasia. J Clin Endocrinol Metab 87:5119-5124
137. O'Shaughnessy PJ, Baker PJ, Monteiro A, Cassie S, Bhattacharya S, Fowler PA (2007) Developmental changes in human fetal testicular cell numbers and messenger ribonucleic acid levels during the second trimester. J Clin Endocrinol Metab 92:4792-4801
138. Ojeda SJ (2004) Female reproductive function. In: Griffin JE, Ojeda SR (eds) Textbook of endocrine physiology. Oxford University Press, Oxford, pp 186-225
139. Ostner J, Heistermann M, Kappeler PM (2003) Intersexual dominance, masculinized genitals and prenatal steroids: comparative data from lemurid primates. Naturwissenschaften 90:141-144
140. Pardridge WM, Gorski RA, Lippe BM, Green R (1982) Androgens and sexual behavior. Ann Intern Med 96:488-501
141. Pasterski VL, Geffner ME, Brain C, Hindmarsh P, Brook C, Hines M (2005) Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia. Child Dev 76:264-278
142. Pattison JC, Abbott DH, Saltzman W, Nguyen AD, Henderson G, Jing H, Pryce CR, Allen AJ, Conley AJ, Bird IM (2005) Male marmoset monkeys express an adrenal fetal zone at birth, but not a zona reticularis in adulthood. Endocrinology 146:365-374
143. Pepe GJ, Albrecht ED (1995) Actions of placental and fetal adrenal steroid hormones in primate pregnancy. Endocr Rev 16:608-648
144. Pereira ME, Fairbanks LA (2002) Juvenile primates: life history, development, and behavior. Oxford University Press, New York, p 461
145. Philibert P, Audran F, Pienkowski C, Morange I, Kohler B, Flori E, Heinrich C, Dacou-Voutetakis C, Joseph MG, Guedj AM, Journel H, Hecart-Bruna AC, Khotchali I, Ten S, Bouchard P, Paris F, Sultan C (2010) Complete androgen insensitivity syndrome is frequently due to premature stop codons in exon 1 of the androgen receptor gene: an international collaborative report of 13 new mutations. Fertil Steril 94:472-476
146. Phoenix CH, Goy RW, Gerall AA, Young WC (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65:369-382
147. Pomerantz SM, Roy MM, Thornton JE, Goy RW (1985) Expression of adult female patterns of sexual behavior by male, female, and pseudohermaphroditic female rhesus monkeys. Biol Reprod 33:878-889
148. Pomerantz SM, Goy RW, Roy MM (1986) Expression of male-typical behavior in adult female pseudohermaphroditic rhesus: comparisons with normal males and neonatally gonadectomized males and females. Horm Behav 20:483-500
149. Power TG (2000)Play and exploration in children and animals. Lawrence Erlbaum Associations, London, p 497
150. Prahalada S, Tarantal AF, Harris GS, Ellsworth KP, Clarke AP, Skiles GL, MacKenzie KI, Kruk LF, Ablin DS, Cukierski MA, Peter CP, vanZwieten MJ, Hendrickx AG (1997) Effects of finasteride, a type 2 5-alpha reductase inhibitor, on fetal development in the rhesus monkey (Macaca mulatta). Teratology 55:119-131
151. Rabinovici J, Jaffe RB (1990) Development and regulation of growth and differentiated function in human and subhuman primate fetal gonads. Endocr Rev 11:532-557
152. Randall DJ, Burggren W, French K (2002)Eckert animal physiology. W.H. Freeman & Company, New York, p 752
153. Rao AJ, Kotagi SG (1983) Serum testosterone levels during the menstrual cycle and early pregnancy in the bonnet monkey (Macaca radiata). Endocrinol Jpn 29:271-275
154. Resko JA (1985) Gonadal hormones during sexual differentiation in vertebrates. In: Goy RW (ed) Handbook of behavioral neurobiology. Plenum, New York, pp 21-42
155. Resko JA, Ellinwood W (1981) Testicular hormone production in fetal rhesus macaques. In: Novy MJ, Resko JA (eds) Fetal endocrinology. Academic, New York, pp 253-267
156. Resko JA, Ellinwood WE (1984) Sexual differentiation of the brain of primates. In: Serio M, Motta M, Zanisi M, Martini L (eds) Sexual differentiation: basic and clinical aspects. Raven, New York, pp 169-181
157. Resko JA, Roselli CE (1997) Prenatal hormones organize sex differences of the neuroendocrine reproductive system: observations on guinea pigs and nonhuman primates. Cell Mol Neurobiol 17:627-648
158. Resko JA, Buhl AE, Phoenix CH (1987) Treatment of pregnant rhesus macaques with testosterone propionate: observations on its fate in the fetus. Biol Reprod 37:1185-1191
159. Reyes FI, Winter JSD, Faiman C (1973) Studies on human sexual development: I. Fetal gonadal and adrenal sex steroids. J Clin Endocrinol Metab 37:74-78
160. Richmond EJ, Rogol AD (2007) Male pubertal development and the role of androgen therapy. Nat Clin Pract Endocrinol Metab 3:338-344
161. Rivarola MA, Forest MG, Migeon CJ (1968) Testosterone, androstenedione and dehydroepiandrosterone in plasma during pregnancy and at delivery: concentration and protein binding. J Clin Endocrinol Metab 28:34-40
162. Rodeck CH, Gill D, Rosenberg DA, Collins WP (1985) Testosterone levels in midtrimester maternal and fetal plasma and amniotic fluid. Prenat Diagn 5:175-181
163. Ross CN, French JA, Patera KJ (2004) Intensity of aggressive interactions modulates testosterone in male marmosets. Physiol Behav 83:437-445
164. Ross CN, Fite JE, Jensen HA, French JA (2007a) Demographic review of a captive colony of Callitrichids (Callithrix kuhlii). Am J Primatol 69:234-240
165. Ross CN, French JA, Orti G (2007b) Germ-line chimerism and paternal care in marmosets (Callithrix kuhlii). Proc Natl Acad Sci USA 104:6278-6282
166. Rouiller-Fabre V, Muczynski V, Lambrot R, Lécureuil C, Coffigny H, Pairault C, Moison D, Angenard G, Bakalska M, Courtot A, Frydman R, Habert R (2009)Ontogenesis of testicular function in humans. Folia Histochem Cytobiol 47:S19-S24
167. Saez JM, Forest MG, Morera AM, Bertrand J (1972) Metabolic clearance rate and blood production rate of testosterone and dihydrotestosterone in normal subjects, during pregnancy, and in hyperthyroidism. J Clin Invest 51:1226-1234
168. Sanchez-Morgado JM, Haworth R, Morris TH (2003) XY female marmoset (Callithrix jacchus). Comp Med 53:539-544
169. Seidman SN (2003) The aging male: androgens, erectile dysfunction, and depression. J Clin Psychiatry 64:31-37
170. Seidman SN (2007) Androgens and the aging male. Psyhcopharmacol Bull 40:205-218
171. Siiteri PK, MacDonald PC (1963) The utilization of circulating dehydroepiandrosterone sulfate for estrogen synthesis during human pregnancy. Steroids 2:713-730
172. 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. Hum Reprod 17:2573-2579
173. Sir-Petermann T, Hitchsfeld C, Maliqueo M, Codner E, Echiburú B, Gazitúa R, Recabarren S, Cassorla F (2005) Birth weight in offspring of mothers with polycystic ovarian syndrome. Hum Reprod 20:2122-2126
174. Sir-Petermann T, Codner E, Perez V, Echiburu B, Maliqueo M, Ladron de Guevara A, Preisler J, Crisosto N, Sanchez F, Cassorla F, Bhasin S (2009) Metabolic and reproductive features before and during puberty in daughters of women with polycystic ovary syndrome. J Clin Endocrinol Metab 94:1923-1930
175. Sivakumaran S, Zhang J, Kelley KMM, Gonit M, Hao H, Ratnam M (2010) Androgen activation of the folate receptor a gene through partial tethering of the androgen receptor by C/EBP a . J Steroid Biochem Mol Biol 122:333-340
176. Smith AS, Birnie AK, French JA (2010) Maternal androgen levels during pregnancy are associated with early-life growth in Geoffroy's marmosets, Callithrix geoffroyi. Gen Comp Endocrinol 166:307-313
177. Stanczyk FZ (2006) Diagnosis of hyperandrogenism: biochemical criteria. Best Pract Res Clin Endocrinol Metab 20:177-191
178. Stearns SC (1992)The evolution of life histories. Oxford University Press, Oxford, p 249
179. Steier JA, Ulstein M, Myking OL (2002) Human chorionic gonadotropin and testosterone in normal and preeclamptic pregnancies in relation to fetal sex. Obstet Gynecol 100:552-556
180. Steiner RA, Bremner WJ (1981) Endocrine correlates of sexual development in the male monkey, Macaca fascicularis. Endocrinology 109:914-919
181. Stevenson MF, Poole TB (1982) Playful interactions in family groups of the common marmoset (Callithrix jacchus jacchus). Anim Behav 30:886-900
182. Stoinski TS, Czekala N, Lukas KE, Maple TL (2002) Urinary androgen and corticoid levels in captive, male Western lowland gorillas (Gorilla g. gorilla): age- and social group-related differences. Am J Primatol 56:73-87
183. Svechnikov K, Söder O (2008) Ontogeny of gonadal sex steroids. Best Pract Res Clin Endocrinol Metab 22:95-106
184. Svechnikov K, Izzo G, Landreh L, Weisser J, Söder O (2010) Endocrine disruptors and Leydig cell function. J Biomed Biotechnol 2010:684504
185. Tapanainen J, Kellokumpu-Lehtinen P, Pelliniemi L, Huhtaniemi I (1981) Age-related changes in endogenous steroids of human fetal testis during early and midpregnancy. J Clin Endocrinol Metab 52:98-102
186. Thornton J, Goy RW (1986) Female-typical sexual behavior of rhesus and defeminization by androgens given prenatally. Horm Behav 20:129-147
187. Thornton J, Zehr JL, Loose MD (2009) Effects of prenatal androgens on rhesus monkeys: a model system to explore the organizational hypothesis in primates. Horm Behav 55:633-644
188. Tomaszycki ML, Davis JE, Gouzoules H, Wallen K (2001) Sex differences in infant rhesus macaque separation-rejection vocalizations and effects of prenatal androgens. Horm Behav 39:267-276
189. Troisi R, Potischman N, Roberts JM, Siiteri P, Daftary A, Sims C, Hoover RN (2003) Associations of maternal and umbilical cord hormone concentrations with maternal, gestational and neonatal factors (United States). Cancer Causes Control 14:347-355
190. 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
191. van de Beek C, Thijssen JHH, Cohen-Kettenis PT, van Goozen SHM, Buitelaar JK (2004) Relationships between sex hormones assessed in amniotic fluid, and maternal and umbilical cord serum: what is the best source of information to investigate the effects of fetal hormonal exposure? Horm Behav 46:663-669
192. van de Beek C, van Goozen S, Buitelaar J, Cohen-Kettenis P (2009) Prenatal sex hormones (maternal and amniotic fluid) and gender-related play behavior in 13-month-old infants. Arch Sex Behav 38:6-15
193. van Wagenen G, Simpson ME (1965) Embryology of the ovary and testes in Homo sapiens and Macaca mulatta. Yale University Press, New Haven, 256 pp
194. Vanky E, Stridsklev S, Skogøy K, Kleggetveit O, Hjelle S, Brandis PV, Eikeland T, Flo K, Berg KF, Bunford G, Lund A, Bjerke C, Almås I, Berg AH, Danielsson A, Lahmami G, Carlsen SM (2010) PCOS - what matters in early pregnancy? - data from a cross-sectional, multicenter study. Acta Obstet Gynecol Scand 90:398-404
195. Vorona E, Zitzmann M, Gromoll J, Schuring AN, Nieschlag E (2007) Clinical, endocrinological, and epigenetic features of the 46, XX male syndrome, compared with 47, XXY Klinefelter patients. J Clin Endocrinol Metab 92:3458-3465
196. Wagenknecht LE, Langefeld CD, Scherzinger AL, Norris JM, Haffner SM, Saad MF, Bergman RN (2003) Insulin sensitivity, insulin secretion, and abdominal fat: The Insulin Resistance Atherosclerosis Study (IRAS) Family Study. Diabetes 52:2490-2496
197. Wallen K (2005) Hormonal in fluences on sexually differentiated behavior in nonhuman primates. Front Neuroendocrinol 26:7-26
198. Wallen K, Hassett JM (2009) Sexual differentiation of behaviour in monkeys: role of prenatal hormones. J Neuroendocrinol 21:421-426
199. Watts DP, Pusey AE (2002) Behavior of juvenile and adolescent great apes. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, New York, pp 148-156
200. Werner R, Grotsch H, Hiort O (2010) 46, XY disorders of sex development - the undermasculinised male with disorders of androgen action. Best Pract Res Clin Endocrinol Metab 24:263-277
201. White PC, Speiser PW (2000) Congenital adrenal hyperplasia due to 21-hydroxylase de ficiency. Endocr Rev 21:245-291
202. Whitehouse AJO, Maybery MT, Hart R, Sloboda DM, Stanley FJ, Newnham JP, Hickey M (2010)Free testosterone levels in umbilical-cord blood predict infant head circumference in females. Dev Med Child Neurol 52:E73-E77
203. Wilson JD, Griffin JE, Russell DW (1993) Steroid 5 alpha-reductase 2 de ficiency. Endocr Rev 14:577-593
204. Winborn WB, Sheridan PJ, McGill HC (1987) Sex steroid receptors in the stomach, liver, pancreas, and gastrointestinal tract of the baboon. Gastroenterology 92:23-32
205. Wisniewski AB, Mazur T (2009)46,XY DSD with female or ambiguous external genitalia at birth due to androgen insensitivity syndrome, 5alpha-reductase-2 de ficiency, or 17beta-hydroxysteroid dehydrogenase de ficiency: A review of quality of life outcomes. Int J Pediatr Endocrino 2009: 567430
206. Xita N, Tsatsoulis A (2006) Fetal programming of polycystic ovary syndrome by androgen excess: evidence from experimental, clinical, and genetic association studies. J Clin Endocrinol Metab 91:1660-1666
207. Yamamoto ME (1993) From dependence to sexual maturity: the behavioural ontogeny of Callitrichidae. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford University Press, New York, pp 235-254
208. Yki-Järvinen H, Koivisto VA (1983) Effects of body composition on insulin sensitivity. Diabetes 32:965-969
209. Young WC, Goy RW, Phoenix CH (1964) Hormones and sexual behavior. Science 143:212-218
210. Zehr JL, Van Meter PE, Wallen K (2005) Factors regulating the timing of puberty onset in female rhesus monkeys (Macaca mulatta): role of prenatal androgens, social rank, and adolescent body weight. Biol Reprod 72:1087-1094