Placental hormones and the control of maternal metabolism and fetal growth

Current Opinion in Endocrinology, Diabetes and Obesity

Volumn 18, Issue 6, 2011, Pages 409-416

  Newbern, Dorothee ^a   Freemark, Michael ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

growth hormone; insulin; insulin like growth factor; placental lactogen; prolactin

Indexed keywords

GROWTH HORMONE; HUMAN PLACENTA LACTOGEN; HYPOPHYSIS HORMONE; LEPTIN; PLACENTA GROWTH HORMONE; PLACENTAL PEPTIDE HORMONE; PROLACTIN; UNCLASSIFIED DRUG;

CELL EXPANSION; FETUS GROWTH; FOOD INTAKE; GENE EXPRESSION REGULATION; HORMONE ACTION; HUMAN; INSULIN RESISTANCE; INSULIN SYNTHESIS; METABOLIC REGULATION; NONHUMAN; NUTRIENT DYNAMICS; NUTRIENT UPTAKE; PANCREAS ISLET BETA CELL; PREGNANCY DIABETES MELLITUS; REVIEW; SIGNAL TRANSDUCTION;

ADIPOKINES; FEMALE; FETAL DEVELOPMENT; FETUS; GLUCOCORTICOIDS; HUMANS; INSULIN; LEPTIN; MATERNAL-FETAL EXCHANGE; PITUITARY GLAND; PLACENTA; PLACENTAL HORMONES; PREGNANCY;

EID: 80255134522     PISSN: 1752296X     EISSN: 17522978     Source Type: Journal    
DOI: 10.1097/MED.0b013e32834c800d     Document Type: Review

References (71)

1. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008; 359:61-73.
2. Highman TJ, Friedman JE, Huston LP, et al. Longitudinal changes in maternal serum leptin concentrations, body composition, and resting metabolic rate in pregnancy. Am J Obstet Gynecol 1998; 178:1010-1015. (Pubitemid 28247179)
3. Masuzaki H, Ogawa Y, Sagawa N, et al. Nonadipose tissue production of leptin: leptin as a novel placenta-derived hormone in humans. Nat Med 1997; 3:1029-1033. (Pubitemid 27391961)
4. Freemark M. Regulation of maternal metabolism by pituitary and placental hormones: roles in fetal development and metabolic programming. Horm Res Paediatr 2006; 65 (Suppl 3):41-49. (Pubitemid 44689432)
5. Kirwan JP, Hauguel-De Mouzon S, Lepercq J, et al. TNF-a is a predictor of insulin resistance in human pregnancy. Diabetes 2002; 51:2207-2213. (Pubitemid 34729026)
6. Catalano PM, Hoegh M, Minium J, et al. Adiponectin in human pregnancy: implications for regulation of glucose and lipid metabolism. Diabetologia 2006; 49:1677-1685. (Pubitemid 43848106)
7. Murphy VE, Smith R, Giles WB, Clifton VL. Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocr Rev 2006; 27:141-169.
8. Freemark M, Driscoll P, Andrews J, et al. Ontogenesis of prolactin receptor gene expression in the rat olfactory system: potential roles for lactogenic hormones in olfactory development. Endocrinology 1996; 137:934-942. (Pubitemid 26070371)
9. Shingo T, Gregg C, Enwere E, et al. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003; 299:117-120. (Pubitemid 36042416)
10. Bridges RS, Freemark MS. Human placental lactogen infusions into the medial preoptic area stimulate maternal behavior in steroid-primed, nulliparous female rats. Horm Behav 1995; 29:216-226.
11. Das A, Mantena SR, Kannan A, et al. De novo synthesis of estrogen in pregnant uterus is critical for stromal decidualization and angiogenesis. Proc Natl Acad Sci U S A 2009; 106:12542-12547.
12. Reynolds LP, Borowicz PP, Caton JS, et al. Uteroplacental vascular development and placental function: an update. Int J Dev Biol 2010; 54:355-366.
13. Augustine RA, Grattan DR. Induction of central leptin resistance in hyperphagic pseudopregnant rats by chronic prolactin infusion. Endocrinology 2008; 149:1049-1055. (Pubitemid 351397926)
14. Druckmann R, Druckmann MA. Progesterone and the immunology of pregnancy. J Steroid Biochem Mol Biol 2005; 97:389-396. (Pubitemid 41691876)
15. Mastorakos G, Ilias I. Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Ann N Y Acad Sci 2003; 997:136-149. (Pubitemid 38491069)
16. Ryan EA, Enns L. Role of gestational hormones in the induction of insulin resistance. J Clin Endocrinol Metab 1988; 67:341-347.
17. Fuglsang J, Ovesen P. Aspects of placental growth hormone physiology. Growth Horm IGF Res 2006; 16:67-85.
18. Baumann GP. Growth hormone isoforms. Growth Horm IGF Res 2009; 19:333-340.
19. Vickers MH, Gilmour S, Gertler A, et al. 20-kDa placental hGH-V has diminished diabetogenic and lactogenic activities compared with 22-kDa hGH-N while retaining antilipogenic activity. Am J Physiol Endocrinol Metab 2009; 297:E629-E637.
20. Fuglsang J. Ghrelin in pregnancy and lactation. Vitam Horm 2008; 77:259-284.
21. Alsat E, Guibourdenche J, Couturier A, Evain-Brion D. Physiological role of human placental growth hormone. Mol Cell Endocrinol 1998; 140:121-127. (Pubitemid 28375222)
22. Lacroix MC, Guibourdenche J, Frendo JL, et al. Human placental growth hormone: a review. Placenta 2002; 23 (Suppl 1):S87-S94. (Pubitemid 39658618)
23. Alsat E, Guibourdenche J, Luton D, et al. Human placental growth hormone. Am J Obstet Gynecol 1997; 177:1526-1534. (Pubitemid 28040255)
24. Grattan DR, Steyn FJ, Kokay IC, et al. Pregnancy-induced adaptation in the neuroendocrine control of prolactin secretion. J Neuroendocrinol 2008; 20:497-507. (Pubitemid 351437035)
25. Tyson JE, Austin K, Farinholt J, Fiedler J. Endocrine-metabolic response to acute starvation in human gestation. Am J Obstet Gynecol 1976; 125:1073-1084.
26. Trujillo ML, Spuch C, Carro E, Senaris R. Hyperphagia and central mechanisms for leptin resistance during pregnancy. Endocrinology 2011; 152: 1355-1365.
27. Strader AD, Buntin JD. Changes in agouti-related peptide during the ring dove breeding cycle in relation to prolactin and parental hyperphagia. J Neuroendocrinol 2003; 15:1046-1053. (Pubitemid 37369165)
28. Li C, Chen P, Smith MS. Neuropeptide Y and tuberoinfundibular dopamine activities are altered during lactation: role of prolactin. Endocrinology 1999; 140:118-123. (Pubitemid 29011149)
29. Igout A, Frankenne F, LHermite-Baleriaux M, et al. Somatogenic and lactogenic activity of the recombinant 22 kDa isoform of human placental growth hormone. Growth Regul 1995; 5:60-65.
30. Caufriez A, Frankenne F, Hennen G, Copinschi G. Regulation of maternal IGF-I by placental GH in normal and abnormal human pregnancies. Am J Physiol Endocrinol Metab 1993; 265:E572-E577.
31. Barbour LA, Shao J, Qiao L, et al. Human placental growth hormone increases expression of the P85 regulatory unit of phosphatidylinositol 3-kinase and triggers severe insulin resistance in skeletal muscle. Endocrinology 2004; 145:1144-1150. (Pubitemid 38280994)
32. Barbour LA, Shao J, Qiao L, et al. Human placental growth hormone causes severe insulin resistance in transgenic mice. Am J Obstet Gynecol 2002; 186:512-517. (Pubitemid 34234166)
33. Verhaeghe J, Bougoussa M, Van Herck E, et al. Placental growth hormone and IGF-I in a pregnant woman with Pit-1 deficiency. Clin Endocrinol (Oxf) 2000; 53:645-647.
34. Barbour LA, Mizanoor Rahman S, Gurevich I, et al. Increased P85alpha is a potent negative regulator of skeletal muscle insulin signaling and induces in vivo insulin resistance associated with growth hormone excess. J Biol Chem 2005; 280:37489-37494. (Pubitemid 41642357)
35. Barbour LA, McCurdy CE, Hernandez TL, et al. Cellular mechanisms for insulin resistance in normal pregnancy and gestational diabetes. Diabetes Care 2007; 30 (Suppl 2):S112-S119. (Pubitemid 47036412)
36. Zavalza-Gómez AB, Anaya-Prado R, Rincón-Sánchez AR, Mora-Martínez JM. Adipokines and insulin resistance during pregnancy. Diabetes Res Clin Pract 2008; 80:8-15.
37. Meier JJ, Butler AE, Saisho Y, et al. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 2008; 57:1584-1594.
38. Arumugam R, Horowitz E, Lu D, et al. The interplay of prolactin and the glucocorticoids in the regulation of {beta}-cell gene expression, fatty acid oxidation, and glucose-stimulated insulin secretion: implications for carbohydrate metabolism in pregnancy. Endocrinology 2008; 149:5401-5414.
39. Arumugam R, Fleenor D, Lu D, Freemark M. Differential and complementary effects of glucose and prolactin on islet DNA synthesis and gene expression. Endocrinology 2011; 152:856-868.
40. Fujinaka Y, Takane K, Yamashita H, Vasavada RC. Lactogens promote beta cell survival through JAK2/STAT5 activation and Bcl-XL upregulation. J Biol Chem 2007; 282:30707-30717. (Pubitemid 350035214)
41. Fleenor D, Petryk A, Driscoll P, Freemark M. Constitutive expression of placental lactogen in pancreatic beta cells: effects on cell morphology, growth, and gene expression. Pediatr Res 2000; 47:136-142. (Pubitemid 30038903)
42. Vasavada RC, Garcia-Ocana A, Zawalich WS, et al. Targeted expression of placental lactogen in the beta cells of transgenic mice results in beta cell proliferation, islet mass augmentation, and hypoglycemia. J Biol Chem 2000; 275:15399-15406. (Pubitemid 30337270)
43. Freemark M, Avril I, Fleenor D, et al. Targeted deletion of the PRL receptor: effects on islet development, insulin production, and glucose tolerance. Endocrinology 2002; 143:1378-1385. (Pubitemid 34274368)
44. Huang C, Snider F, Cross JC. Prolactin receptor is required for normal glucose homeostasis and modulation of {beta}-cell mass during pregnancy. Endocrinology 2009; 150:1618-1626.
45. Arumugam R, Horowitz E, Noland RC, et al. Regulation of islet {beta}-cell pyruvate metabolism: interactions of prolactin, glucose, and dexamethasone. Endocrinology 2010; 151:3074-3083.
46. Kim H, Toyofuku Y, Lynn FC, et al. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 2010; 16:804-808. doi: 10.1038/nm. 2173.
47. Schraenen A, Lemaire K, de Faudeur G, et al. Placental lactogens induce serotonin biosynthesis in a subset of mouse beta cells during pregnancy. Diabetologia 2010; 53:2589-2599.
48. Kushner JA, Ciemerych MA, Sicinska E, et al. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 2005; 25:3752-3762. (Pubitemid 40559580)
49. Georgia S, Bhushan A. Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J Clin Invest 2004; 114:963-968. (Pubitemid 39578724)
50. Rieck S, White P, Schug J, et al. The transcriptional response of the islet to pregnancy in mice. Mol Endocrinol 2009; 23:1702-1712.
51. Heinonen S, Taipale P, Saarikoski S. Weights of placentae from small-forgestational age infants revisited. Placenta 2001; 22:399-404. (Pubitemid 32519789)
52. Ursell W, Brudenell M, Chard T. Placental lactogen levels in diabetic pregnancy. Br Med J 1973; 2:80-82.
53. McIntyre HD, Serek R, Crane DI, et al. Placental growth hormone (GH), GHbinding protein, and insulin-like growth factor axis in normal, growth-retarded, and diabetic pregnancies: correlations with fetal growth. J Clin Endocrinol Metab 2000; 85:1143-1150. (Pubitemid 32269363)
54. Mittal P, Espinoza J, Hassan S, et al. Placental growth hormone is increased in the maternal and fetal serum of patients with preeclampsia. J Matern Fetal Neonatal Med 2007; 20:651-659. (Pubitemid 47262701)
55. Mirlesse V, Frankenne F, Alsat E, et al. Placental growth hormone levels in normal pregnancy and in pregnancies with intrauterine growth retardation. Pediatr Res 1993; 34:439-442. (Pubitemid 23297171)
56. Leger J, Noel M, Limal JM, Czernichow P. Growth factors and intrauterine growth retardation. II. Serum growth hormone, insulin-like growth factor (IGF) I, and IGF-binding protein 3 levels in children with intrauterine growth retardation compared with normal control subjects: prospective study from birth to two years of age. Study Group of IUGR. Pediatr Res 1996; 40:101-107.
57. Setia S, Sridhar MG. Changes in GH/IGF-1 axis in intrauterine growth retardation: consequences of fetal programming? Horm Metab Res 2009; 41:791-798.
58. Koutsaki M, Sifakis S, Zaravinos A, et al. Decreased placental expression of hPGH, IGF-I and IGFBP-1 in pregnancies complicated by fetal growth restriction. Growth Horm IGF Res 2011; 21:31-36.
59. Mannik J, Vaas P, Rull K, et al. Differential expression profile of growth hormone/chorionic somatomammotropin genes in placenta of small-and large-for-gestational-age newborns. J Clin Endocrinol Metab 2010; 95: 2433-2442.
60. Bock JE, Gaede P, Trolle D. Human placental lactogen hormone in serum from pregnant women with rhesus (anti-D) isoimmunization. Acta Obstet Gynecol Scand Suppl 1976; 53:14-19.
61. Nielsen PV, Pedersen H, Kampmann EM. Absence of human placental lactogen in an otherwise uneventful pregnancy. Am J Obstet Gynecol 1979; 135:322-326. (Pubitemid 9253633)
62. Wurzel JM, Parks JS, Herd JE, Nielsen PV. A gene deletion is responsible for absence of human chorionic somatomammotropin. DNA 1982; 1:251-257. (Pubitemid 13172024)
63. Borody IB, Carlton MA. Isolated defect in human placental lactogen synthesis in a normal pregnancy. Case report. Br J Obstet Gynaecol 1981; 88:447-449. (Pubitemid 11113119)
64. Alexander I, Anthony F, Letchworth AT. PLacental protein profile and glucose studies in a normal pregnancy with extremely low levels of human placental lactogen. Case report. Br J Obstet Gynaecol 1982; 89:241-243. (Pubitemid 12192930)
65. Sideri M, De Virgiliis G, Guidobono F, et al. Immunologically undetectable human placental lactogen in a normal pregnancy. Case report. Br J Obstet Gynaecol 1983; 90:771-773. (Pubitemid 13031760)
66. Wohlk P, Nexo E, Jorgensen EH, et al. Low or absent serum placental lactogen hormone in 2 normal pregnancies. Ugeskr Laeger 1984; 146: 727-729.
67. Barbieri F, Botticelli A, Consarino R, et al. Failure of placenta to produce hPL in an otherwise uneventful pregnancy: a case report. Biol Res Pregnancy Perinatol 1986; 7:131-133. (Pubitemid 17193468)
68. Simon P, Decoster C, Brocas H, et al. Absence of human chorionic somatomammotropin during pregnancy associated with two types of gene deletion. Hum Genet 1986; 74:235-238. (Pubitemid 17056541)
69. Trapp M, De Wilde R, Holzgreve W, et al. A pregnancy without detectable human placental lactogen (hPL). Zentralbl Gynakol 1987; 109:130-133.
70. Rygaard K, Revol A, Esquivel-Escobedo D, et al. Absence of human placental lactogen and placental growth hormone (HGH-V) during pregnancy: PCR analysis of the deletion. Hum Genet 1998; 102:87-92. (Pubitemid 28185266)
71. Fleenor D, Oden J, Kelly PA, et al. Roles of the lactogens and somatogens in perinatal and postnatal metabolism and growth: studies of a novel mouse model combining lactogen resistance and growth hormone deficiency. Endocrinology 2005; 146:103-112. (Pubitemid 40051729)