Intrauterine environment and polycystic ovary syndrome

Seminars in Reproductive Medicine

Volumn 32, Issue 3, 2014, Pages 159-165

  Dumesic, Daniel A ^a   Goodarzi, Mark O ^b   Chazenbalk, Gregorio D ^a   Abbott, David H ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

adiposity; developmental programming; fetal development; hyperandrogenism; hyperinsulinemia; polycystic ovary syndrome

Indexed keywords

ANDROGEN; TESTOSTERONE;

ADULT DISEASE; ANDROGEN BLOOD LEVEL; ARTICLE; BIRTH; CLINICAL STUDY; CONGENITAL ADRENAL HYPERPLASIA; DISEASE COURSE; DISEASE PREDISPOSITION; DNA MODIFICATION; ENDOCRINE DISEASE; EPIGENETICS; FETUS (ANATOMY); FETUS DEVELOPMENT; GENETIC SUSCEPTIBILITY; GESTATION PERIOD; HUMAN; METABOLIC DISORDER; MOTHER; MOTHER FETUS RELATIONSHIP; NONHUMAN; ONTOGENY; OVARY POLYCYSTIC DISEASE; PHENOTYPE; PREGNANCY DIABETES MELLITUS; PROGENY; REPRODUCTION; SECOND TRIMESTER PREGNANCY; UTERUS; FEMALE; FETOMATERNAL TRANSFUSION; PATHOPHYSIOLOGY; PHYSIOLOGY; POLYCYSTIC OVARY SYNDROME; PREGNANCY;

FEMALE; HUMANS; MATERNAL-FETAL EXCHANGE; POLYCYSTIC OVARY SYNDROME; PREGNANCY; UTERUS;

EID: 84898449731     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0034-1371087     Document Type: Article

References (89)

1. Zawadzki J., Dunaif A. Diagnostic criteria for polycystic ovary syndrome: towards a rational approach. In: Dunaif A., Givens J. R., Haseltine F. P., Merriam G. R., eds. Polycystic Ovary Syndrome. Boston, MA Blackwell Scientific: 1992; 377 384
2. Azziz R., Marin C., Hoq L., Badamgarav E., Song P. Health care-related economic burden of the polycystic ovary syndrome during the reproductive life span. J Clin Endocrinol Metab: 2005; 90 8 4650 4658 (Pubitemid 41159355)
3. Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod: 2004; 19 1 41 47
4. Azziz R., Woods K. S., Reyna R., Key T. J., Knochenhauer E. S., Yildiz B. O. The prevalence and features of the polycystic ovary syndrome in an unselected population. J Clin Endocrinol Metab: 2004; 89 6 2745 2749 (Pubitemid 38766360)
5. Fauser B. CJM, Tarlatzis B. C., Rebar R. W., et al. Consensus on women's health aspects of polycystic ovary syndrome (PCOS): the Amsterdam ESHRE/ASRM-Sponsored 3rd PCOS Consensus Workshop Group. Fertil Steril: 2012; 97 1 28 38, e25
6. March W. A., Moore V. M., Willson K. J., Phillips D. IW, Norman R. J., Davies M. J. The prevalence of polycystic ovary syndrome in a community sample assessed under contrasting diagnostic criteria. Hum Reprod: 2010; 25 2 544 551
7. Carmina E., Chu M. C., Longo R. A., Rini G. B., Lobo R. A. Phenotypic variation in hyperandrogenic women influences the findings of abnormal metabolic and cardiovascular risk parameters. J Clin Endocrinol Metab: 2005; 90 5 2545 2549 (Pubitemid 40686289)
8. Welt C. K., Gudmundsson J. A., Arason G., et al. Characterizing discrete subsets of polycystic ovary syndrome as defined by the Rotterdam criteria: the impact of weight on phenotype and metabolic features. J Clin Endocrinol Metab: 2006; 91 12 4842 4848 (Pubitemid 44917316)
9. Azziz R., Carmina E., Dewailly D., et al. Androgen Excess Society. Positions statement: criteria for defining polycystic ovary syndrome as a predominantly hyperandrogenic syndrome: an Androgen Excess Society guideline. J Clin Endocrinol Metab: 2006; 91 11 4237 4245 (Pubitemid 44833391)
10. Barnes R. B., Rosenfield R. L., Ehrmann D. A., et al. Ovarian hyperandrogynism as a result of congenital adrenal virilizing disorders: evidence for perinatal masculinization of neuroendocrine function in women. J Clin Endocrinol Metab: 1994; 79 5 1328 1333 (Pubitemid 24369843)
11. Merke D. P., Cutler G. B. Jr. New ideas for medical treatment of congenital adrenal hyperplasia. Endocrinol Metab Clin North Am: 2001; 30 1 121 135 (Pubitemid 32381717)
12. Phocas I., Chryssikopoulos A., Sarandakou A., Rizos D., Trakakis E. A contribution to the classification of cases of non-classic 21-hydroxylase- deficient congenital adrenal hyperplasia. Gynecol Endocrinol: 1995; 9 3 229 238
13. Stikkelbroeck N. M., Hermus A. R., Braat D. D., Otten B. J. Fertility in women with congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Obstet Gynecol Surv: 2003; 58 4 275 284 (Pubitemid 36407196)
14. Dumesic D. A., Abbott D. H., Padmanabhan V. Polycystic ovary syndrome and its developmental origins. Rev Endocr Metab Disord: 2007; 8 127 141 (Pubitemid 47434646)
15. Kuijper E. AM, Vink J. M., Lambalk C. B., Boomsma D. I. Prevalence of polycystic ovary syndrome in women from opposite-sex twin pairs. J Clin Endocrinol Metab: 2009; 94 6 1987 1990
16. Cattrall F. R., Vollenhoven B. J., Weston G. C. Anatomical evidence for in utero androgen exposure in women with polycystic ovary syndrome. Fertil Steril: 2005; 84 6 1689 1692 (Pubitemid 41785665)
17. Palomba S., Marotta R., Di Cello A., et al. Pervasive developmental disorders in children of hyperandrogenic women with polycystic ovary syndrome: a longitudinal case-control study. Clin Endocrinol (Oxf): 2012; 77 6 898 904
18. Lujan M. E., Bloski T. G., Chizen D. R., Lehotay D. C., Pierson R. A. Digit ratios do not serve as anatomical evidence of prenatal androgen exposure in clinical phenotypes of polycystic ovary syndrome. Hum Reprod: 2010; 25 1 204 211
19. Lujan M. E., Podolski A. J., Chizen D. R., Lehotay D. C., Pierson R. A. Digit ratios by computer-assisted analysis confirm lack of anatomical evidence of prenatal androgen exposure in clinical phenotypes of polycystic ovary syndrome. Reprod Biol Endocrinol: 2010; 8 156 163
20. Lutchmaya S., Baron-Cohen S., Raggatt P., Knickmeyer R., Manning J. T. 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Hum Dev: 2004; 77 1-2 23 28 (Pubitemid 38534445)
21. Abbott A. D., Colman R. J., Tiefenthaler R., Dumesic D. A., Abbott D. H. Early-to-mid gestation fetal testosterone increases right hand 2D:4D finger length ratio in polycystic ovary syndrome-like monkeys. PLoS ONE: 2012; 7 8 e42372
22. Barry J. A., Kay A. R., Navaratnarajah R., et al. Umbilical vein testosterone in female infants born to mothers with polycystic ovary syndrome is elevated to male levels. J Obstet Gynaecol: 2010; 30 5 444 446
23. Mehrabian F., Kelishadi R. Comparison of the metabolic parameters and androgen level of umbilical cord blood in newborns of mothers with polycystic ovary syndrome and controls. J Res Med Sci: 2012; 17 3 207 211
24. Anderson H., Fogel N., Grebe S. K., Singh R. J., Taylor R. L., Dunaif A. Infants of women with polycystic ovary syndrome have lower cord blood androstenedione and estradiol levels. J Clin Endocrinol Metab: 2010; 95 5 2180 2186
25. Maliqueo M., Lara H. E., Sánchez F., Echiburú B., Crisosto N., Sir-Petermann T. Placental steroidogenesis in pregnant women with polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol: 2013; 166 2 151 155
26. Hickey M., Sloboda D. M., Atkinson H. C., et al. The relationship between maternal and umbilical cord androgen levels and polycystic ovary syndrome in adolescence: a prospective cohort study. J Clin Endocrinol Metab: 2009; 94 10 3714 3720
27. Cole B., Hensinger K., Maciel G. AR, Chang R. J., Erickson G. F. Human fetal ovary development involves the spatiotemporal expression of p450c17 protein. J Clin Endocrinol Metab: 2006; 91 9 3654 3661 (Pubitemid 44402151)
28. Mesiano S. The endocrinology of human pregnancy and fetoplacental neuroendocrine development. In: Strauss J. F. III, Barbieri R. L., eds. Yen and Jaffe's Reproductive Endocrinology: Physiology, Pathophysiology, and Clinical Management. 6th ed. Philadelphia, PA Saunders Elsevier: 2009; 248 281
29. Fowler P. A., Anderson R. A., Saunders P. T., et al. Development of steroid signaling pathways during primordial follicle formation in the human fetal ovary. J Clin Endocrinol Metab: 2011; 96 6 1754 1762
30. van de Beek C., Thijssen J. HH, Cohen-Kettenis P. T., van Goozen S. HM, Buitelaar J. K. 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: 2004; 46 5 663 669 (Pubitemid 39535148)
31. Goodarzi M. O., Dumesic D. A., Chazenbalk G., Azziz R. Polycystic ovary syndrome: etiology, pathogenesis and diagnosis. Nat Rev Endocrinol: 2011; 7 4 219 231
32. Adashi E. Y. The ovarian follicular apparatus. In: Adashi E. Y., Rock J. A., Rosenwaks Z., eds. Reproductive Endocrinology, Surgery, and Technology. Philadelphia, PA Lippincott-Raven: 1996; 18 40
33. Hatzirodos N., Bayne R. A., Irving-Rodgers H. F., et al. Linkage of regulators of TGF-β activity in the fetal ovary to polycystic ovary syndrome. FASEB J: 2011; 25 7 2256 2265
34. Voutilainen R., Miller W. L. Developmental expression of genes for the stereoidogenic enzymes P450scc (20,22-desmolase), P450c17 (17 alpha-hydroxylase/17,20-lyase), and P450c21 (21-hydroxylase) in the human fetus. J Clin Endocrinol Metab: 1986; 63 5 1145 1150 (Pubitemid 17173052)
35. Shifren J. L., Osathanondh R., Yeh J. Human fetal ovaries and uteri: developmental expression of genes encoding the insulin, insulin-like growth factor I, and insulin-like growth factor II receptors. Fertil Steril: 1993; 59 5 1036 1040 (Pubitemid 23139675)
36. Payne A. H., Jaffe R. B. Androgen formation from pregnenolone sulfate by the human fetal ovary. J Clin Endocrinol Metab: 1974; 39 2 300 304
37. Wilson E. A., Jawad M. J. The effect of trophic agents on fetal ovarian steroidogenesis in organ culture. Fertil Steril: 1979; 32 1 73 79 (Pubitemid 9187971)
38. George F. W., Wilson J. D. Conversion of androgen to estrogen by the human fetal ovary. J Clin Endocrinol Metab: 1978; 47 3 550 555 (Pubitemid 9010405)
39. Pepe G. J., Billiar R. B., Albrecht E. D. Regulation of baboon fetal ovarian folliculogenesis by estrogen. Mol Cell Endocrinol: 2006; 247 1-2 41 46 (Pubitemid 43277706)
40. Albrecht E. D., Pepe G. J. Estrogen regulation of placental angiogenesis and fetal ovarian development during primate pregnancy. Int J Dev Biol: 2010; 54 2-3 397 408
41. Reyes F. I., Winter J. S., Faiman C. Studies on human sexual development. I. Fetal gonadal and adrenal sex steroids. J Clin Endocrinol Metab: 1973; 37 1 74 78
42. Beck-Peccoz P., Padmanabhan V., Baggiani A. M., et al. Maturation of hypothalamic-pituitary-gonadal function in normal human fetuses: circulating levels of gonadotropins, their common alpha-subunit and free testosterone, and discrepancy between immunological and biological activities of circulating follicle-stimulating hormone. J Clin Endocrinol Metab: 1991; 73 3 525 532 (Pubitemid 21921904)
43. Barbieri R. L., Saltzman D. H., Torday J. S., Randall R. W., Frigoletto F. D., Ryan K. J. Elevated concentrations of the β-subunit of human chorionic gonadotropin and testosterone in the amniotic fluid of gestations of diabetic mothers. Am J Obstet Gynecol: 1986; 154 5 1039 1043 (Pubitemid 16085724)
44. Driscoll S. G., Benirschke K., Curtis G. W. Neonatal deaths among infants of diabetic mothers. Postmortem findings in ninety-five infants. Am J Dis Child: 1960; 100 818 835
45. Hultquist G. T., Olding L. B. Endocrine pathology of infants of diabetic mothers. A quantitative morphological analysis including a comparison with infants of iso-immunized and of non-diabetic mothers. Acta Endocrinol Suppl (Copenh): 1981; 241 (Suppl): 1 202
46. Sir-Petermann T., Maliqueo M., Angel B., Lara H. E., Pérez-Bravo F., Recabarren S. E. Maternal serum androgens in pregnant women with polycystic ovarian syndrome: possible implications in prenatal androgenization. Hum Reprod: 2002; 17 10 2573 2579 (Pubitemid 35174106)
47. Boomsma C. M., Eijkemans M. JC, Hughes E. G., Visser G. HA, Fauser B. CJM, Macklon N. S. A meta-analysis of pregnancy outcomes in women with polycystic ovary syndrome. Hum Reprod Update: 2006; 12 6 673 683 (Pubitemid 44605508)
48. Kjerulff L. E., Sanchez-Ramos L., Duffy D. Pregnancy outcomes in women with polycystic ovary syndrome: a metaanalysis. Am J Obstet Gynecol: 2011; 204 1 6
49. Altieri P., Gambineri A., Prontera O., Cionci G., Franchina M., Pasquali R. Maternal polycystic ovary syndrome may be associated with adverse pregnancy outcomes. Eur J Obstet Gynecol Reprod Biol: 2010; 149 1 31 36
50. Bjercke S., Dale P. O., Tanbo T., Storeng R., Ertzeid G., Abyholm T. Impact of insulin resistance on pregnancy complications and outcome in women with polycystic ovary syndrome. Gynecol Obstet Invest: 2002; 54 2 94 98 (Pubitemid 36164639)
51. Abbott D. H., Bruns C. R., Barnett D. K., et al. Experimentally-induced gestational androgen excess disrupts glucoregulation in rhesus monkey dams and their female offspring. Am J Physiol Endocrinol Metab: 2010; 299 E741 E751
52. Padmanabhan V., Veiga-Lopez A. Developmental origin of reproductive and metabolic dysfunctions: androgenic versus estrogenic reprogramming. Semin Reprod Med: 2011; 29 3 173 186
53. Sir-Petermann T., Codner E., Maliqueo M., et al. Increased anti-Müllerian hormone serum concentrations in prepubertal daughters of women with polycystic ovary syndrome. J Clin Endocrinol Metab: 2006; 91 8 3105 3109 (Pubitemid 44271764)
54. Crisosto N., Echiburú B., Maliqueo M., et al. Improvement of hyperandrogenism and hyperinsulinemia during pregnancy in women with polycystic ovary syndrome: possible effect in the ovarian follicular mass of their daughters. Fertil Steril: 2012; 97 1 218 224
55. Maliqueo M., Echiburú B., Crisosto N., et al. Metabolic parameters in cord blood of newborns of women with polycystic ovary syndrome. Fertil Steril: 2009; 92 1 277 282
56. Crisosto N., Codner E., Maliqueo M., et al. Anti-Müllerian hormone levels in peripubertal daughters of women with polycystic ovary syndrome. J Clin Endocrinol Metab: 2007; 92 7 2739 2743 (Pubitemid 47037384)
57. Kent S. C., Gnatuk C. L., Kunselman A. R., Demers L. M., Lee P. A., Legro R. S. Hyperandrogenism and hyperinsulinism in children of women with polycystic ovary syndrome: a controlled study. J Clin Endocrinol Metab: 2008; 93 5 1662 1669 (Pubitemid 351656502)
58. Sir-Petermann T., Codner E., Pérez V., et al. Metabolic and reproductive features before and during puberty in daughters of women with polycystic ovary syndrome. J Clin Endocrinol Metab: 2009; 94 6 1923 1930
59. Yamamoto M., Feigenbaum S. L., Crites Y., et al. Risk of preterm delivery in non-diabetic women with polycystic ovarian syndrome. J Perinatol: 2012; 32 10 770 776
60. Cresswell J. L., Barker D. J., Osmond C., Egger P., Phillips D. I., Fraser R. B. Fetal growth, length of gestation, and polycystic ovaries in adult life. Lancet: 1997; 350 9085 1131 1135 (Pubitemid 27454005)
61. Mumm H., Kamper-Jorgensen M., Nybo Andersen A. M., Glintborg D., Andersen M. Birth weight and polycystic ovary syndrome in adult life: a register-based study on 523,757 Danish women born 1973-1991. Fertil Steril: 2013; 99 3 777 782
62. Sir-Petermann T., Hitchsfeld C., Maliqueo M., et al. Birth weight in offspring of mothers with polycystic ovarian syndrome. Hum Reprod: 2005; 20 8 2122 2126 (Pubitemid 41418494)
63. Ibáñez L., Potau N., Francois I., de Zegher F. Precocious pubarche, hyperinsulinism, and ovarian hyperandrogenism in girls: relation to reduced fetal growth. J Clin Endocrinol Metab: 1998; 83 10 3558 3562 (Pubitemid 28500889)
64. Legro R. S., Roller R. L., Dodson W. C., Stetter C. M., Kunselman A. R., Dunaif A. Associations of birthweight and gestational age with reproductive and metabolic phenotypes in women with polycystic ovarian syndrome and their first-degree relatives. J Clin Endocrinol Metab: 2010; 95 2 789 799
65. Laitinen J., Taponen S., Martikainen H., et al. Body size from birth to adulthood as a predictor of self-reported polycystic ovary syndrome symptoms. Int J Obes Relat Metab Disord: 2003; 27 6 710 715 (Pubitemid 36712955)
66. Haakova L., Cibula D., Rezabek K., Hill M., Fanta M., Zivny J. Pregnancy outcome in women with PCOS and in controls matched by age and weight. Hum Reprod: 2003; 18 7 1438 1441 (Pubitemid 36840951)
67. Mikola M., Hiilesmaa V., Halttunen M., Suhonen L., Tiitinen A. Obstetric outcome in women with polycystic ovarian syndrome. Hum Reprod: 2001; 16 2 226 229 (Pubitemid 32149412)
68. Chazenbalk G. D., Aguilera P., Keller E., Dumesic D. A., Abbott D. H. Altered transition of adipose stem cell commitment to early preadipocyte differentiation in subcutaneous abdominal adipose tissue of adult PCOS-like female rhesus monkeys. Paper presented at the 95th Annual Meeting of the Endocrine Society; June 15-18, 2013; San Francisco, CA, Poster Mon-555
69. Chazenbalk G., Singh P., Irge D., Shah A., Abbott D. H., Dumesic D. A. Androgens inhibit adipogenesis during human adipose stem cell commitment to preadipocyte formation. Steroids: 2013; 78 9 920 926
70. Heneidi S., Simerman A. A., Keller E., et al. Awakened by cellular stress: isolation and characterization of a novel population of pluripotent stem cells derived from human adipose tissue. PLoS ONE: 2013; 8 6 e64752
71. Legro R. S., Driscoll D., Strauss J. F. III, Fox J., Dunaif A. Evidence for a genetic basis for hyperandrogenemia in polycystic ovary syndrome. Proc Natl Acad Sci U S A: 1998; 95 25 14956 14960 (Pubitemid 29003738)
72. Kahsar-Miller M. D., Nixon C., Boots L. R., Go R. C., Azziz R. Prevalence of polycystic ovary syndrome (PCOS) in first-degree relatives of patients with PCOS. Fertil Steril: 2001; 75 1 53 58 (Pubitemid 32042114)
73. Vink J. M., Sadrzadeh S., Lambalk C. B., Boomsma D. I. Heritability of polycystic ovary syndrome in a Dutch twin-family study. J Clin Endocrinol Metab: 2006; 91 6 2100 2104 (Pubitemid 43854989)
74. Chen Z. J., Zhao H., He L., et al. Genome-wide association study identifies susceptibility loci for polycystic ovary syndrome on chromosome 2p16.3, 2p21 and 9q33.3. Nat Genet: 2011; 43 1 55 59
75. Shi Y., Zhao H., Shi Y., et al. Genome-wide association study identifies eight new risk loci for polycystic ovary syndrome. Nat Genet: 2012; 44 9 1020 1025
76. Zeggini E., Scott L. J., Saxena R., et al. Wellcome Trust Case Control Consortium. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet: 2008; 40 5 638 645 (Pubitemid 351601209)
77. Voight B. F., Scott L. J., Steinthorsdottir V., et al. MAGIC investigators; GIANT Consortium. Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat Genet: 2010; 42 7 579 589
78. Hakonarson H., Qu H. Q., Bradfield J. P., et al. A novel susceptibility locus for type 1 diabetes on Chr12q13 identified by a genome-wide association study. Diabetes: 2008; 57 4 1143 1146
79. Lango Allen H., Estrada K., Lettre G., et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature: 2010; 467 7317 832 838
80. Fox C. S., Heard-Costa N., Cupples L. A., Dupuis J., Vasan R. S., Atwood L. D. Genome-wide association to body mass index and waist circumference: the Framingham Heart Study 100K project. BMC Med Genet: 2007; 8 01 S18
81. Díaz-Perales A., Quesada V., Sánchez L. M., et al. Identification of human aminopeptidase O, a novel metalloprotease with structural similarity to aminopeptidase B and leukotriene A4 hydrolase. J Biol Chem: 2005; 280 14 14310 14317 (Pubitemid 40517334)
82. Li Z., Huang H. Epigenetic abnormality: a possible mechanism underlying the fetal origin of polycystic ovary syndrome. Med Hypotheses: 2008; 70 3 638 642 (Pubitemid 351193031)
83. Zhu J. Q., Zhu L., Liang X. W., Xing F. Q., Schatten H., Sun Q. Y. Demethylation of LHR in dehydroepiandrosterone-induced mouse model of polycystic ovary syndrome. Mol Hum Reprod: 2010; 16 4 260 266
84. Qu F., Wang F. F., Yin R., et al. A molecular mechanism underlying ovarian dysfunction of polycystic ovary syndrome: hyperandrogenism induces epigenetic alterations in the granulosa cells. J Mol Med (Berl): 2012; 90 8 911 923
85. Xu N., Kwon S., Abbott D. H., et al. Epigenetic mechanism underlying the development of polycystic ovary syndrome (PCOS)-like phenotypes in prenatally androgenized rhesus monkeys. PLoS ONE: 2011; 6 11 e27286
86. Dos Santos E., Dieudonné M. N., Leneveu M. C., Pecquery R., Serazin V., Giudicelli Y. In vitro effects of chorionic gonadotropin hormone on human adipose development. J Endocrinol: 2007; 194 2 313 325 (Pubitemid 47249670)
87. Park B. H., Kim Y. J., Park J. S., et al. Folate and homocysteine levels during pregnancy affect DNA methylation in human placenta [in Korean]. J Prev Med Pub Health: 2005; 38 4 437 442
88. Rees W. D., Wilson F. A., Maloney C. A. Sulfur amino acid metabolism in pregnancy: the impact of methionine in the maternal diet. J Nutr: 2006; 136 (6, Suppl): 1701S 1705S (Pubitemid 43765383)
89. Kwong W. Y., Miller D. J., Wilkins A. P., et al. Maternal low protein diet restricted to the preimplantation period induces a gender-specific change on hepatic gene expression in rat fetuses. Mol Reprod Dev: 2007; 74 1 48 56 (Pubitemid 44846356)