Adaptability and potential for treatment of placental functions to improve embryonic development and postnatal health
James C. Cross
+ Author Affiliations
- Author Affiliations
Departments of Comparative Biology and Experimental Medicine, Biochemistry and Molecular Biology, Medical Genetics, and Obstetrics and Gynecology, University of Calgary, Calgary, Alberta T2N 4N1, Canada. Email: jcross@ucalgary.ca
Reproduction, Fertility and Development 28(2) 75-82 https://doi.org/10.1071/RD15342
Published: 3 December 2015
Abstract
For an organ that is so critical for life in eutherian mammals, the placenta hardly gets the attention that it deserves. The placenta does a series of remarkable things, including implanting the embryo in the uterus, negotiating with the mother for nutrients but also protecting her health during pregnancy, helping establish normal metabolic and cardiovascular function for life postnatally (developmental programming) and initiating changes that prepare the mother to care for and suckle her young after birth. Different lines of evidence in experimental animals suggest that the development and function of the placenta are adaptable. This means that some of the changes observed in pathological pregnancies may represent attempts to mitigate the impact of fetal growth and development. Key and emerging concepts are reviewed here concerning how we may view the placenta diagnostically and therapeutically in pregnancy complications, focusing on information from experimental studies in mice, sheep and cattle, as well as association studies from humans. Hundreds of different genes have been shown to underlie normal placental development and function, some of which have promise as tractable targets for intervention in pregnancies at risk for poor fetal growth.
Additional keywords: fetal growth, nutrition, placenta, pregnancy, trophoblast.
References
Adamson, S. L., Lu, Y., Whiteley, K. J., Holmyard, D., Hemberger, M., Pfarrer, C., and Cross, J. C. (2002). Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev. Biol. 250, 358–373.| Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsFSnt74%3D&md5=d4fde3a47588af840b96e7dd2496bd93CAS | 12376109PubMed |
Anderson, C. M., Lopez, F., Zhang, H. Y., Pavlish, K., and Benoit, J. N. (2005). Reduced uteroplacental perfusion alters uterine arcuate artery function in the pregnant Sprague-Dawley rat. Biol. Reprod. 72, 762–766.
| Reduced uteroplacental perfusion alters uterine arcuate artery function in the pregnant Sprague-Dawley rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVeisbs%3D&md5=4356ec8d4794d84ebc2a34b2d16d89f1CAS | 15564595PubMed |
Anson-Cartwright, L., Dawson, K., Holmyard, D., Fisher, S. J., Lazzarini, R. A., and Cross, J. C. (2000). The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 25, 311–314.
| The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvFKks74%3D&md5=d86a6e11fb3f6b7519133c47c41182bbCAS | 10888880PubMed |
Bainbridge, S. A., Minhas, A., Whiteley, K. J., Qu, D., Sled, J. G., Kingdom, J. C., and Adamson, S. L. (2012). Effects of reduced Gcm1 expression on trophoblast morphology, fetoplacental vascularity, and pregnancy outcomes in mice. Hypertension 59, 732–739.
| Effects of reduced Gcm1 expression on trophoblast morphology, fetoplacental vascularity, and pregnancy outcomes in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XisVygsbY%3D&md5=559ee855b768b5b4ef51a10a322c3d80CAS | 22275534PubMed |
Barbour, L. A., Shao, J., Qiao, L., Pulawa, L. K., Jensen, D. R., Bartke, A., Garrity, M., Draznin, B., and Friedman, J. E. (2002). Human placental growth hormone causes severe insulin resistance in transgenic mice. Am. J. Obstet. Gynecol. 186, 512–517.
| Human placental growth hormone causes severe insulin resistance in transgenic mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFCrtrg%3D&md5=5c69424a22907daa47b132b7bd0d4401CAS | 11904616PubMed |
Barbour, L. A., Shao, J., Qiao, L., Leitner, W., Anderson, M., Friedman, J. E., and Draznin, B. (2004). Human placental growth hormone increases expression of the p85 regulatory unit of phosphatidylinositol 3-kinase and triggers severe insulin resistance in skeletal muscle. Endocrinology 145, 1144–1150.
| Human placental growth hormone increases expression of the p85 regulatory unit of phosphatidylinositol 3-kinase and triggers severe insulin resistance in skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1WisLg%3D&md5=2c2f36e753d85c3655dba260d99f9555CAS | 14633976PubMed |
Bell, A. W., and Bauman, D. E. (1997). Adaptations of glucose metabolism during pregnancy and lactation. J. Mammary Gland Biol. Neoplasia 2, 265–278.
| Adaptations of glucose metabolism during pregnancy and lactation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czosF2htg%3D%3D&md5=92d7d32ef916a35a32a7a3e92698678cCAS | 10882310PubMed |
Billestrup, N., and Nielsen, J. H. (1991). The stimulatory effect of growth hormone, prolactin, and placental lactogen on beta-cell proliferation is not mediated by insulin-like growth factor-I. Endocrinology 129, 883–888.
| The stimulatory effect of growth hormone, prolactin, and placental lactogen on beta-cell proliferation is not mediated by insulin-like growth factor-I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltVKmtLk%3D&md5=0d4d3b15a4a68eb0e1a76b0970c6cb96CAS | 1677331PubMed |
Brănişteanu, D. D., and Mathieu, C. (2003). Progesterone in gestational diabetes mellitus: guilty or not guilty? Trends Endocrinol. Metab. 14, 54–56.
| Progesterone in gestational diabetes mellitus: guilty or not guilty?Crossref | GoogleScholarGoogle Scholar | 12591170PubMed |
Braun, T., Li, S., Moss, T. J., Newnham, J. P., Challis, J. R., Gluckman, P. D., and Sloboda, D. M. (2007). Maternal betamethasone administration reduces binucleate cell number and placental lactogen in sheep. J. Endocrinol. 194, 337–347.
| Maternal betamethasone administration reduces binucleate cell number and placental lactogen in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsFenu7g%3D&md5=9029cec8531c1ef4610bed9a24464c76CAS | 17641283PubMed |
Braunstein, G. D., Mills, J. L., Reed, G. F., Jovanovic, L. G., Holmes, L. B., Aarons, J., and Simpson, J. L. (1989). Comparison of serum placental protein hormone levels in diabetic and normal pregnancy. J. Clin. Endocrinol. Metab. 68, 3–8.
| Comparison of serum placental protein hormone levels in diabetic and normal pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2FnvFygtQ%3D%3D&md5=5557ddfa00e4fae781f662f2ac648aa6CAS | 2783318PubMed |
Brelje, T. C., Scharp, D. W., Lacy, P. E., Ogren, L., Talamantes, F., Robertson, M., Friesen, H. G., and Sorenson, R. L. (1993). Effect of homologous placental lactogens, prolactins, and growth hormones on islet B-cell division and insulin secretion in rat, mouse, and human islets: implication for placental lactogen regulation of islet function during pregnancy. Endocrinology 132, 879–887.
| 1:CAS:528:DyaK3sXitVGlsLk%3D&md5=5af6e041d16f77c17e8e7b9264cab340CAS | 8425500PubMed |
Brelje, T. C., Parsons, J. A., and Sorenson, R. L. (1994). Regulation of islet beta-cell proliferation by prolactin in rat islets. Diabetes 43, 263–273.
| Regulation of islet beta-cell proliferation by prolactin in rat islets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFCit7s%3D&md5=227eff885109cee2295bdb69f435e9faCAS | 7904577PubMed |
Burton, G. J., and Fowden, A. L. (2012). Review: the placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta 33, S23–S27.
| Review: the placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation.Crossref | GoogleScholarGoogle Scholar | 22154688PubMed |
Bustamante, J. J., Dai, G., and Soares, M. J. (2008). Pregnancy and lactation modulate maternal splenic growth and development of the erythroid lineage in the rat and mouse. Reprod. Fertil. Dev. 20, 303–310.
| Pregnancy and lactation modulate maternal splenic growth and development of the erythroid lineage in the rat and mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXislyqtbc%3D&md5=2a9fabc59d5ce51024767c23b1265a3eCAS | 18255020PubMed |
Bustamante, J. J., Copple, B. L., Soares, M. J., and Dai, G. (2010). Gene profiling of maternal hepatic adaptations to pregnancy. Liver Int. 30, 406–415.
| Gene profiling of maternal hepatic adaptations to pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1Wkur0%3D&md5=9346db0a0b5edd7f7554a9a2eeee1030CAS | 20040050PubMed |
Carr, D. J., Wallace, J. M., Aitken, R. P., Milne, J. S., Mehta, V., Martin, J. F., Zachary, I. C., Peebles, D. M., and David, A. L. (2014). Uteroplacental adenovirus vascular endothelial growth factor gene therapy increases fetal growth velocity in growth-restricted sheep pregnancies. Hum. Gene Ther. 25, 375–384.
| Uteroplacental adenovirus vascular endothelial growth factor gene therapy increases fetal growth velocity in growth-restricted sheep pregnancies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsFWlt7Y%3D&md5=58a8aa33bef02b4ec5de77577311f2b7CAS | 24593228PubMed |
Chen, J., Tan, B., Karteris, E., Zervou, S., Digby, J., Hillhouse, E. W., Vatish, M., and Randeva, H. S. (2006). Secretion of adiponectin by human placenta: differential modulation of adiponectin and its receptors by cytokines. Diabetologia 49, 1292–1302.
| Secretion of adiponectin by human placenta: differential modulation of adiponectin and its receptors by cytokines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlalur4%3D&md5=8b2eabe9b8c50bd518f057512dd68a1dCAS | 16570162PubMed |
Chen, P. Y., Ganguly, A., Rubbi, L., Orozco, L. D., Morselli, M., Ashraf, D., Jaroszewicz, A., Feng, S., Jacobsen, S. E., Nakano, A., Devaskar, S. U., and Pellegrini, M. (2013). Intrauterine calorie restriction affects placental DNA methylation and gene expression. Physiol. Genomics 45, 565–576.
| Intrauterine calorie restriction affects placental DNA methylation and gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1OmtLjL&md5=5bc28e942f14a0b4937a917a660df603CAS | 23695884PubMed |
Chesnutt, A. N. (2004). Physiology of normal pregnancy. Crit. Care Clin. 20, 609–615.
| Physiology of normal pregnancy.Crossref | GoogleScholarGoogle Scholar | 15388191PubMed |
Coan, P. M., Vaughan, O. R., Sekita, Y., Finn, S. L., Burton, G. J., Constancia, M., and Fowden, A. L. (2010). Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J. Physiol. 588, 527–538.
| Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvV2js7o%3D&md5=1bc2acdda65dfad083927b24dab896d3CAS | 19948659PubMed |
Coan, P. M., Vaughan, O. R., McCarthy, J., Mactier, C., Burton, G. J., Constancia, M., and Fowden, A. L. (2011). Dietary composition programmes placental phenotype in mice. J. Physiol. 589, 3659–3670.
| Dietary composition programmes placental phenotype in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsl2qu74%3D&md5=bea76e1a036d8ec075367432b3d99741CAS | 21624969PubMed |
Constância, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C., and Reik, W. (2002). Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417, 945–948.
| Placental-specific IGF-II is a major modulator of placental and fetal growth.Crossref | GoogleScholarGoogle Scholar | 12087403PubMed |
Cross, J. C. (1996). Trophoblast function in normal and preeclamptic pregnancy. Fetal Matern. Med. Rev. 8, 57–66.
| Trophoblast function in normal and preeclamptic pregnancy.Crossref | GoogleScholarGoogle Scholar |
Cross, J. C., and Mickelson, L. (2006). Nutritional influences on implantation and placental development. Nutr. Rev. 64, S12–S18.
| Nutritional influences on implantation and placental development.Crossref | GoogleScholarGoogle Scholar | 16770948PubMed |
Cross, J. C., Werb, Z., and Fisher, S. J. (1994). Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508–1518.
| Implantation and the placenta: key pieces of the development puzzle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisVGmu78%3D&md5=963658a9d2e4152a5609e87c06b33651CAS | 7985020PubMed |
Danilovich, N., Wernsing, D., Coschigano, K. T., Kopchick, J. J., and Bartke, A. (1999). Deficits in female reproductive function in GH-R-KO mice; role of IGF-I. Endocrinology 140, 2637–2640.
| Deficits in female reproductive function in GH-R-KO mice; role of IGF-I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtlKhtL0%3D&md5=0bda48bf5f2e8707120f26de03f276a7CAS | 10342852PubMed |
de Boo, H. A., Eremia, S. C., Bloomfield, F. H., Oliver, M. H., and Harding, J. E. (2008). Treatment of intrauterine growth restriction with maternal growth hormone supplementation in sheep. Am. J. Obstet. Gynecol. 199, 559e1–9.
| Treatment of intrauterine growth restriction with maternal growth hormone supplementation in sheep.Crossref | GoogleScholarGoogle Scholar |
del Rincon, J. P., Iida, K., Gaylinn, B. D., McCurdy, C. E., Leitner, J. W., Barbour, L. A., Kopchick, J. J., Friedman, J. E., Draznin, B., and Thorner, M. O. (2007). Growth hormone regulation of p85alpha expression and phosphoinositide 3-kinase activity in adipose tissue: mechanism for growth hormone-mediated insulin resistance. Diabetes 56, 1638–1646.
| Growth hormone regulation of p85alpha expression and phosphoinositide 3-kinase activity in adipose tissue: mechanism for growth hormone-mediated insulin resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtlKhs7w%3D&md5=1266d0d8d537f47f9d7b33e313211b98CAS | 17363744PubMed |
Devlieger, R., Casteels, K., and Van Assche, F. A. (2008). Reduced adaptation of the pancreatic B cells during pregnancy is the major causal factor for gestational diabetes: current knowledge and metabolic effects on the offspring. Acta Obstet. Gynecol. Scand. 87, 1266–1270.
| Reduced adaptation of the pancreatic B cells during pregnancy is the major causal factor for gestational diabetes: current knowledge and metabolic effects on the offspring.Crossref | GoogleScholarGoogle Scholar | 18846453PubMed |
Eggan, K., Akutsu, H., Loring, J., Jackson-Grusby, L., Klemm, M., Rideout, W. M., Yanagimachi, R., and Jaenisch, R. (2001). Hybrid vigor, fetal overgrowth, and viability of mice derived by nuclear cloning and tetraploid embryo complementation. Proc. Natl Acad. Sci. USA 98, 6209–6214.
| Hybrid vigor, fetal overgrowth, and viability of mice derived by nuclear cloning and tetraploid embryo complementation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzhtlCgtg%3D%3D&md5=7dc3d4ef5cf4ae7fb866485885c6b663CAS | 11331774PubMed |
Fasshauer, M., Bluher, M., and Stumvoll, M. (2014). Adipokines in gestational diabetes. Lancet Diabetes Endocrinol. 2, 488–499.
| Adipokines in gestational diabetes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXptVaqsLs%3D&md5=87273a61b91c8cff8edd66718027b590CAS | 24731659PubMed |
Frías, J. L., Frías, J. P., Frías, P. A., and Martínez-Frías, M. L. (2007). Infrequently studied congenital anomalies as clues to the diagnosis of maternal diabetes mellitus. Am. J. Med. Genet. A. 143A, 2904–2909.
| Infrequently studied congenital anomalies as clues to the diagnosis of maternal diabetes mellitus.Crossref | GoogleScholarGoogle Scholar | 18000913PubMed |
Gluckman, P. D., and Hanson, M. A. (2004). The developmental origins of the metabolic syndrome. Trends Endocrinol. Metab. 15, 183–187.
| The developmental origins of the metabolic syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsVegurk%3D&md5=8e12351796f6d89106fed4bb17553f28CAS | 15109618PubMed |
Gluckman, P. D., and Harding, J. E. (1997). The physiology and pathophysiology of intrauterine growth retardation. Horm. Res. 48, 11–16.
| The physiology and pathophysiology of intrauterine growth retardation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjt1Kjurk%3D&md5=1f67566eaac9112e740c169e0f1d3255CAS | 9161866PubMed |
Gootwine, E. (2004). Placental hormones and fetal-placental development. Anim. Reprod. Sci. 82-83, 551–566.
| Placental hormones and fetal-placental development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVCitbw%3D&md5=747a4585e143e790bba9032b9e9cb549CAS | 15271479PubMed |
Guillomot, M., Taghouti, G., Constant, F., Degrelle, S., Hue, I., Chavatte-Palmer, P., and Jammes, H. (2010). Abnormal expression of the imprinted gene Phlda2 in cloned bovine placenta. Placenta 31, 482–490.
| Abnormal expression of the imprinted gene Phlda2 in cloned bovine placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVWruro%3D&md5=c0088447d22a06688033aceb3d6c0986CAS | 20381142PubMed |
Hattori, N., Davies, T. C., Anson-Cartwright, L., and Cross, J. C. (2000). Periodic expression of the Cdk inhibitor p57Kip2 in trophoblast giant cells defines a G2-like gap phase of the endocycle. Mol. Biol. Cell 11, 1037–1045.
| Periodic expression of the Cdk inhibitor p57Kip2 in trophoblast giant cells defines a G2-like gap phase of the endocycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjslCisr0%3D&md5=50f17ef5dcb308c7b716cfd5525e2173CAS | 10712518PubMed |
Holt, R. I. (2002). Fetal programming of the growth hormone–insulin-like growth factor axis. Trends Endocrinol. Metab. 13, 392–397.
| Fetal programming of the growth hormone–insulin-like growth factor axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVShsr8%3D&md5=ff2833a575cdc200ff3c908bb2e89f14CAS | 12367821PubMed |
Intapad, S., Warrington, J. P., Spradley, F. T., Palei, A. C., Drummond, H. A., Ryan, M. J., Granger, J. P., and Alexander, B. T. (2014). Reduced uterine perfusion pressure induces hypertension in the pregnant mouse. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307, R1353–R1357.
| Reduced uterine perfusion pressure induces hypertension in the pregnant mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXptVCisg%3D%3D&md5=a4054d27233f42a15e1759456ab00dcdCAS | 25298513PubMed |
Jaquiery, A. L., Oliver, M. H., Rumball, C. W., Bloomfield, F. H., and Harding, J. E. (2009). Undernutrition before mating in ewes impairs the development of insulin resistance during pregnancy. Obstet. Gynecol. 114, 869–876.
| Undernutrition before mating in ewes impairs the development of insulin resistance during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1ylsbjF&md5=a55857d9ea0e9988ef5f72e6509a0d98CAS | 19888047PubMed |
Jones, H. N., Crombleholme, T., and Habli, M. (2013). Adenoviral-mediated placental gene transfer of IGF-1 corrects placental insufficiency via enhanced placental glucose transport mechanisms. PLoS One 8, e74632.
| Adenoviral-mediated placental gene transfer of IGF-1 corrects placental insufficiency via enhanced placental glucose transport mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVCrsr7L&md5=ee7b6a1fe561d61c3d02c0c7bbf96b3cCAS | 24019972PubMed |
Kelly, P. A., Bachelot, A., Kedzia, C., Hennighausen, L., Ormandy, C. J., Kopchick, J. J., and Binart, N. (2002). The role of prolactin and growth hormone in mammary gland development. Mol. Cell. Endocrinol. 197, 127–131.
| The role of prolactin and growth hormone in mammary gland development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosFCmsL8%3D&md5=49232e36b9dd4770b46a113577b558ddCAS | 12431805PubMed |
Kingdom, J. C. P., and Kaufmann, P. (1997). Oxygen and placental villous development: origins of fetal hypoxia. Placenta 18, 613–621.
| Oxygen and placental villous development: origins of fetal hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FjtFWkuw%3D%3D&md5=f08d0b9fe965fe2892d3ee8af3ba090cCAS |
Kooistra, H. S., and Okkens, A. C. (2001). Secretion of prolactin and growth hormone in relation to ovarian activity in the dog. Reprod. Domest. Anim. 36, 115–119.
| Secretion of prolactin and growth hormone in relation to ovarian activity in the dog.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVygtL0%3D&md5=997331890b111dcfe3b15202e319410dCAS | 11555356PubMed |
Larsen, C. M., and Grattan, D. R. (2012). Prolactin, neurogenesis, and maternal behaviors. Brain Behav. Immun. 26, 201–209.
| Prolactin, neurogenesis, and maternal behaviors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yqt7Y%3D&md5=1c68f9aca58c067c3857549f53b90c09CAS | 21820505PubMed |
Lea, R. G., Wooding, P., Stewart, I., Hannah, L. T., Morton, S., Wallace, K., Aitken, R. P., Milne, J. S., Regnault, T. R., Anthony, R. V., and Wallace, J. M. (2007). The expression of ovine placental lactogen, StAR and progesterone-associated steroidogenic enzymes in placentae of overnourished growing adolescent ewes. Reproduction 133, 785–796.
| The expression of ovine placental lactogen, StAR and progesterone-associated steroidogenic enzymes in placentae of overnourished growing adolescent ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFersr4%3D&md5=afa51fe759f38accbe0dc4b07542eb58CAS | 17504922PubMed |
Männik, J., Vaas, P., Rull, K., Teesalu, P., Rebane, T., and Laan, M. (2010). Differential expression profile of growth hormone/chorionic somatomammotropin genes in placenta of small- and large-for-gestational-age newborns. J. Clin. Endocrinol. Metab. 95, 2433–2442.
| Differential expression profile of growth hormone/chorionic somatomammotropin genes in placenta of small- and large-for-gestational-age newborns.Crossref | GoogleScholarGoogle Scholar | 20233782PubMed |
McIntyre, H. D., Serek, R., Crane, D. I., Veveris-Lowe, T., Parry, A., Johnson, S., Leung, K. C., Ho, K. K., Bougoussa, M., Hennen, G., Igout, A., Chan, F. Y., Cowley, D., Cotterill, A., and Barnard, R. (2000). Placental growth hormone (GH), GH-binding protein, and insulin-like growth factor axis in normal, growth-retarded, and diabetic pregnancies: correlations with fetal growth. J. Clin. Endocrinol. Metab. 85, 1143–1150.
| 1:CAS:528:DC%2BD3cXisFOqsro%3D&md5=e27825f65ed5a33754680be7bba2b448CAS | 10720053PubMed |
Mirlesse, V., Frankenne, F., Alsat, E., Poncelet, M., Hennen, G., and Evain-Brion, D. (1993). Placental growth hormone levels in normal pregnancy and in pregnancies with intrauterine growth retardation. Pediatr. Res. 34, 439–442.
| Placental growth hormone levels in normal pregnancy and in pregnancies with intrauterine growth retardation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2FnslKitA%3D%3D&md5=a455a5643dfc256d675feac36f62cee7CAS | 8255674PubMed |
Morton, N. E. (1955). The inheritance of human birth weight. Ann. Hum. Genet. 20, 125–134.
| The inheritance of human birth weight.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG28%2FitV2rsw%3D%3D&md5=6d6dcc90b865cce6981886159c11ac03CAS | 13268984PubMed |
Mullis, P. E. (2010). Genetics of isolated growth hormone deficiency. J. Clin. Res. Pediatr. Endocrinol. 2, 52–62.
| Genetics of isolated growth hormone deficiency.Crossref | GoogleScholarGoogle Scholar | 21274339PubMed |
Newbern, D., and Freemark, M. (2011). Placental hormones and the control of maternal metabolism and fetal growth. Curr. Opin. Endocrinol. Diabetes Obes. 18, 409–416.
| Placental hormones and the control of maternal metabolism and fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlKrsb%2FE&md5=d057e603f1cb5f7caa6ec939d1dfc0c3CAS | 21986512PubMed |
Nielsen, J. H. (1982). Effects of growth hormone, prolactin, and placental lactogen on insulin content and release, and deoxyribonucleic acid synthesis in cultured pancreatic islets. Endocrinology 110, 600–606.
| Effects of growth hormone, prolactin, and placental lactogen on insulin content and release, and deoxyribonucleic acid synthesis in cultured pancreatic islets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhtFKht7Y%3D&md5=94919299a0ae5b166a9dac8b44987d04CAS | 6276141PubMed |
Ogura, A., Inoue, K., Ogonuki, N., Lee, J., Kohda, T., and Ishino, F. (2002). Phenotypic effects of somatic cell cloning in the mouse. Cloning Stem Cells 4, 397–405.
| Phenotypic effects of somatic cell cloning in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvFeguw%3D%3D&md5=4b0942fa9c89a567e1dd6de26c9afcebCAS | 12626102PubMed |
Oh-McGinnis, R., Bogutz, A. B., and Lefebvre, L. (2011). Partial loss of Ascl2 function affects all three layers of the mature placenta and causes intrauterine growth restriction. Dev. Biol. 351, 277–286.
| Partial loss of Ascl2 function affects all three layers of the mature placenta and causes intrauterine growth restriction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXit1yltbk%3D&md5=93730c1bbc955b83bb506c34e3c33d59CAS | 21238448PubMed |
Oliver, M. H., Harding, J. E., Breier, B. H., Evans, P. C., and Gluckman, P. D. (1992). The nutritional regulation of circulating placental lactogen in fetal sheep. Pediatr. Res. 31, 520–523.
| The nutritional regulation of circulating placental lactogen in fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVKrurk%3D&md5=8a4b94bf3bbe52c27c5df2a1f41a8e6bCAS | 1603632PubMed |
Oliver, M. H., Hawkins, P., and Harding, J. E. (2005). Periconceptional undernutrition alters growth trajectory and metabolic and endocrine responses to fasting in late-gestation fetal sheep. Pediatr. Res. 57, 591–598.
| Periconceptional undernutrition alters growth trajectory and metabolic and endocrine responses to fasting in late-gestation fetal sheep.Crossref | GoogleScholarGoogle Scholar | 15695605PubMed |
Parsons, J. A., Brelje, T. C., and Sorenson, R. L. (1992). Adaptation of islets of Langerhans to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology 130, 1459–1466.
| 1:CAS:528:DyaK38XhvVygt74%3D&md5=393791b00b320aa3bc49d041ba172c8cCAS | 1537300PubMed |
Penrose, L. S. (1952). Data on the genetics of birth weight. Ann. Eugen. 16, 378–381.
| 1:STN:280:DyaG38%2Fotlantg%3D%3D&md5=fb5d9b923072fa3f37e7831da89b6373CAS | 14953134PubMed |
Pfarrer, C. D., Ruziwa, S. D., Winther, H., Callesen, H., Leiser, R., Schams, D., and Dantzer, V. (2006). Localization of vascular endothelial growth factor (VEGF) and its receptors VEGFR-1 and VEGFR-2 in bovine placentomes from implantation until term. Placenta 27, 889–898.
| Localization of vascular endothelial growth factor (VEGF) and its receptors VEGFR-1 and VEGFR-2 in bovine placentomes from implantation until term.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvF2lsLo%3D&md5=657e25b21f54a12a9f8e040783d5a8bfCAS | 16263165PubMed |
Pijnenborg, R., Vercruysse, L., Verbist, L., and Van Assche, F. A. (1998). Interaction of interstitial trophoblast with placental bed capillaries and venules of normotensive and pre-eclamptic pregnancies. Placenta 19, 569–575.
| Interaction of interstitial trophoblast with placental bed capillaries and venules of normotensive and pre-eclamptic pregnancies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FnsFajsA%3D%3D&md5=7f80acbcbad790a50333712293af3a36CAS | 9859859PubMed |
Poon, L. C., and Nicolaides, K. H. (2014). Early prediction of preeclampsia. Obstet. Gynecol. Int. 2014, 297397.
| Early prediction of preeclampsia.Crossref | GoogleScholarGoogle Scholar | 25136369PubMed |
Rawn, S. M., and Cross, J. C. (2008). The evolution, regulation, and function of placenta-specific genes. Annu. Rev. Cell Dev. Biol. 24, 159–181.
| The evolution, regulation, and function of placenta-specific genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlOgtbbM&md5=c83824330b9b6083dfc4548cc349677bCAS | 18616428PubMed |
Redmer, D. A., Luther, J. S., Milne, J. S., Aitken, R. P., Johnson, M. L., Borowicz, P. P., Borowicz, M. A., Reynolds, L. P., and Wallace, J. M. (2009). Fetoplacental growth and vascular development in overnourished adolescent sheep at Day 50, 90 and 130 of gestation. Reproduction 137, 749–757.
| Fetoplacental growth and vascular development in overnourished adolescent sheep at Day 50, 90 and 130 of gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2ntbc%3D&md5=aee31d8b38a71b6c276ecf8f798dabe7CAS | 19164488PubMed |
Schulz, L. C., Schlitt, J. M., Caesar, G., and Pennington, K. A. (2012). Leptin and the placental response to maternal food restriction during early pregnancy in mice. Biol. Reprod. 87, 120.
| Leptin and the placental response to maternal food restriction during early pregnancy in mice.Crossref | GoogleScholarGoogle Scholar | 22993381PubMed |
Sferruzzi-Perri, A. N., Vaughan, O. R., Coan, P. M., Suciu, M. C., Darbyshire, R., Constancia, M., Burton, G. J., and Fowden, A. L. (2011). Placental-specific Igf2 deficiency alters developmental adaptations to undernutrition in mice. Endocrinology 152, 3202–3212.
| Placental-specific Igf2 deficiency alters developmental adaptations to undernutrition in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVemt7fF&md5=d98b92e5951952e7bad187a937101eb5CAS | 21673101PubMed |
Shaat, N., and Groop, L. (2007). Genetics of gestational diabetes mellitus. Curr. Med. Chem. 14, 569–583.
| Genetics of gestational diabetes mellitus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1yhur4%3D&md5=205662337a4def726faf9d09ddc9cce2CAS | 17346148PubMed |
Shingo, T., Gregg, C., Enwere, E., Fujikawa, H., Hassam, R., Geary, C., Cross, J. C., and Weiss, S. (2003). Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299, 117–120.
| Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpvVensLk%3D&md5=d1bbed0b4b5e7428ccf40fdb5d18a947CAS | 12511652PubMed |
Sibley, C. P., Coan, P. M., Ferguson-Smith, A. C., Dean, W., Hughes, J., Smith, P., Reik, W., Burton, G. J., Fowden, A. L., and Constancia, M. (2004). Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc. Natl Acad. Sci. USA 101, 8204–8208.
| Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslCitLo%3D&md5=2fdfc69ea79977964a5f438537686005CAS | 15150410PubMed |
Steingrímsson, E., Tessarollo, L., Reid, S. W., Jenkins, N. A., and Copeland, N. G. (1998). The bHLH-Zip transcription factor Tfeb is essential for placental vascularization. Development 125, 4607–4616.
| 9806910PubMed |
Su, Y., Liebhaber, S. A., and Cooke, N. E. (2000). The human growth hormone gene cluster locus control region supports position-independent pituitary- and placenta-specific expression in the transgenic mouse. J. Biol. Chem. 275, 7902–7909.
| The human growth hormone gene cluster locus control region supports position-independent pituitary- and placenta-specific expression in the transgenic mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitVyltrs%3D&md5=c12e8754b95e22adf47e3b4be514a340CAS | 10713106PubMed |
Takahashi, K., Kobayashi, T., and Kanayama, N. (2000). p57(Kip2) regulates the proper development of labyrinthine and spongiotrophoblasts. Mol. Hum. Reprod. 6, 1019–1025.
| p57(Kip2) regulates the proper development of labyrinthine and spongiotrophoblasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVejurc%3D&md5=4a4deeb8e847c4ce4aba4edcac0db024CAS | 11044465PubMed |
Torgersen, K. L., and Curran, C. A. (2006). A systematic approach to the physiologic adaptations of pregnancy. Crit. Care Nurs. Q. 29, 2–19.
| A systematic approach to the physiologic adaptations of pregnancy.Crossref | GoogleScholarGoogle Scholar | 16456359PubMed |
Tunster, S. J., Van De Pette, M., and John, R. M. (2014). Isolating the role of elevated Phlda2 in asymmetric late fetal growth restriction in mice. Dis. Model. Mech. 7, 1185–1191.
| Isolating the role of elevated Phlda2 in asymmetric late fetal growth restriction in mice.Crossref | GoogleScholarGoogle Scholar | 25085993PubMed |
Tycko, B. (2006). Imprinted genes in placental growth and obstetric disorders. Cytogenet. Genome Res. 113, 271–278.
| Imprinted genes in placental growth and obstetric disorders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVSqurs%3D&md5=675d3ef7509809c9959676c5305956f7CAS | 16575190PubMed |
Ueno, M., Lee, L. K., Chhabra, A., Kim, Y. J., Sasidharan, R., Van Handel, B., Wang, Y., Kamata, M., Kamran, P., Sereti, K. I., Ardehali, R., Jiang, M., and Mikkola, H. K. (2013). c-Met-dependent multipotent labyrinth trophoblast progenitors establish placental exchange interface. Dev. Cell 27, 373–386.
| c-Met-dependent multipotent labyrinth trophoblast progenitors establish placental exchange interface.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2qtLnN&md5=f2faed0e75f3e33e2f3d998e0284af31CAS | 24286824PubMed |
Ushizawa, K., and Hashizume, K. (2006). Biology of the prolactin family in bovine placenta. II. Bovine prolactin-related proteins: their expression, structure and proposed roles. Anim. Sci. J. 77, 18–27.
| Biology of the prolactin family in bovine placenta. II. Bovine prolactin-related proteins: their expression, structure and proposed roles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFCisr0%3D&md5=62465b0eba900ff1ced067a41098f261CAS |
Wallace, J. M., Bourke, D. A., Aitken, R. P., and Cruickshank, M. A. (1999). Switching maternal dietary intake at the end of the first trimester has profound effects on placental development and fetal growth in adolescent ewes carrying singleton fetuses. Biol. Reprod. 61, 101–110.
| Switching maternal dietary intake at the end of the first trimester has profound effects on placental development and fetal growth in adolescent ewes carrying singleton fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktFKgtbc%3D&md5=a689322ab3f2156e6859fe6d7e143992CAS | 10377037PubMed |
Wallace, J. M., Matsuzaki, M., Milne, J., and Aitken, R. (2006). Late but not early gestational maternal growth hormone treatment increases fetal adiposity in overnourished adolescent sheep. Biol. Reprod. 75, 231–239.
| Late but not early gestational maternal growth hormone treatment increases fetal adiposity in overnourished adolescent sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVWgsLY%3D&md5=410f278672ad8d0344e4260884a74179CAS | 16687645PubMed |
Watson, E. D., and Cross, J. C. (2005). Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20, 180–193.
| Development of structures and transport functions in the mouse placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1GgtrY%3D&md5=264857bdbe9741b5928128372b9bd46eCAS | 15888575PubMed |
Weinhaus, A. J., Stout, L. E., and Sorenson, R. L. (1996). Glucokinase, hexokinase, glucose transporter 2, and glucose metabolism in islets during pregnancy and prolactin-treated islets in vitro: mechanisms for long term up-regulation of islets. Endocrinology 137, 1640–1649.
| 1:CAS:528:DyaK28XisFCrurw%3D&md5=7e87225c92735e91775e702c33764c92CAS | 8612496PubMed |
Wiemers, D. O., Shao, L. J., Ain, R., Dai, G., and Soares, M. J. (2003). The mouse prolactin gene family locus. Endocrinology 144, 313–325.
| The mouse prolactin gene family locus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFSltA%3D%3D&md5=71e95d02e2dbc23725235ac9c080234fCAS | 12488360PubMed |
Wildman, D. E., Chen, C., Erez, O., Grossman, L. I., Goodman, M., and Romero, R. (2006). Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc. Natl Acad. Sci. USA 103, 3203–3208.
| Evolution of the mammalian placenta revealed by phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksF2kt7w%3D&md5=fbbd32003b0c3e3bc781b806a97b8490CAS | 16492730PubMed |
Wooding, F. B. P., and Flint, A. P. F. (1994). Placentation. In: ‘Marshall’s Physiology of Reproduction’, 4th edn. (Ed. G. E. Lamming.) pp. 233–460. (Chapman and Hall: New York.)
Wu, L., de Bruin, A., Saavedra, H. I., Starovic, M., Trimboli, A., Yang, Y., Opavska, J., Wilson, P., Thompson, J. C., Ostrowski, M. C., Rosol, T. J., Woollett, L. A., Weinstein, M., Cross, J. C., Robinson, M. L., and Leone, G. (2003). Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421, 942–947.
| Extra-embryonic function of Rb is essential for embryonic development and viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVKgtLs%3D&md5=fa812d4c8dcebaa82c93a1244f695cd6CAS | 12607001PubMed |
Zhang, P., Wong, C., DePinho, R. A., Harper, J. W., and Elledge, S. J. (1998). Cooperation between the cdk inhibitors p27(KIP1) and p57(KIP2) in the control of tissue growth and development. Genes Dev. 12, 3162–3167.
| Cooperation between the cdk inhibitors p27(KIP1) and p57(KIP2) in the control of tissue growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsVSnsL4%3D&md5=bb2a8f40ea69267c02b3833f78afab32CAS | 9784491PubMed |
Zhang, H., Zhang, J., Pope, C. F., Crawford, L. A., Vasavada, R. C., Jagasia, S. M., and Gannon, M. (2010). Gestational diabetes mellitus resulting from impaired beta-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen. Diabetes 59, 143–152.
| Gestational diabetes mellitus resulting from impaired beta-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen.Crossref | GoogleScholarGoogle Scholar | 19833884PubMed |
