Cited by 160Birth, Development, and HealthPregnancy and preeclampsia studiesGestational Diabetes Research and Management

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The Role of Placental Nutrient Sensing in Maternal-Fetal Resource Allocation1

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Díaz, Paula, Powell, Theresa L., Jansson, Thomas·2014·Biology of Reproduction

DOI 10.1095/biolreprod.114.121798PMC PMC4435028

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Abstract

The placenta mediates maternal-fetal exchange and has historically been regarded as a passive conduit for nutrients. However, emerging evidence suggests that the placenta actively responds to nutritional and metabolic signals from the mother and the fetus. We propose that the placenta integrates a multitude of maternal and fetal nutritional cues with information from intrinsic nutrient-sensing signaling pathways to match fetal demand with maternal supply by regulating maternal physiology, placental growth, and nutrient transport. This process, which we have called placental nutrient sensing, ensures optimal allocation of resources between the mother and the fetus to maximize the chances for propagation of parental genes without jeopardizing maternal health. We suggest that these mechanisms have evolved because of the evolutionary pressures of maternal undernutrition, which result in decreased placental growth and down-regulation of nutrient transporters, thereby limiting fetal growth to ensure maternal survival. These regulatory loops may also function in response to maternal overnutrition, leading to increased placental growth and nutrient transport in cases of maternal obesity or gestational diabetes. Thus, placental nutrient sensing modulates maternal-fetal resource allocation to increase the likelihood of reproductive success. This model implies that the placenta plays a critical role in mediating fetal programming and determining lifelong health.

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Molecular mechanisms of mTOR-mediated translational control
Ma, X. M., & Blenis, J. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2672 · Cited by 2,558
Activation of a metabolic gene regulatory network downstream of mTOR complex 1
Düvel, K., Yecies, J. L., Menon, S., Raman, P., Lipovsky, A. I., Souza, A. L., Triantafellow, E., Ma, Q., Gorski, R., Cleaver, S., et al. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.06.022 · Cited by 2,020
Living with the Past: Evolution, Development, and Patterns of Disease
Gluckman, P. D., & Hanson, M. A. (2004) · Science · doi:10.1126/science.1095292 · Cited by 1,917
Nonadipose tissue production of leptin: Leptin as a novel placenta-derived hormone in humans
Masuzaki, H., Ogawa, Y., Sagawa, N., Hosoda, K., Matsumoto, T., Mise, H., Nishimura, H., Yoshimasa, Y., Tanaka, I., Mori, T., et al. (1997) · Nature Medicine · doi:10.1038/nm0997-1029 · Cited by 1,277
Rheological and Physiological Consequences of Conversion of the Maternal Spiral Arteries for Uteroplacental Blood Flow during Human Pregnancy
Burton, G. J., Woods, A., Jauniaux, E. R. M., & Kingdom, J. C. (2009) · Placenta · doi:10.1016/j.placenta.2009.02.009 · Cited by 1,190
Onset of Maternal Arterial Blood Flow and Placental Oxidative Stress
Jauniaux, E., Watson, A. L., Hempstock, J., Bao, Y.-P., Skepper, J. N., & Burton, G. J. (2000) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)64849-3 · Cited by 1,057
Placental-specific IGF-II is a major modulator of placental and fetal growth
Constância, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C., et al. (2002) · Nature · doi:10.1038/nature00819 · Cited by 1,054
AMPK and mTOR in Cellular Energy Homeostasis and Drug Targets
Inoki, K., Kim, J., & Guan, K. (2011) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134537 · Cited by 818
Disruption of imprinting caused by deletion of the H19 gene region in mice
Leighton, P. A., Ingram, R. S., Eggenschwiler, J. T., Efstratiadis, A., & Tilghman, S. M. (1995) · Nature · doi:10.1038/375034a0 · Cited by 756
TNF-α Is a Predictor of Insulin Resistance in Human Pregnancy
Kirwan, J. P., Hauguel-De Mouzon, S., Lepercq, J., Challier, J.-C., Huston-Presley, L., Friedman, J. E., Kalhan, S. C., & Catalano, P. M. (2002) · Diabetes · doi:10.2337/diabetes.51.7.2207 · Cited by 738
Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2Preprint
Thorvaldsen, J. L., Duran, K. L., & Bartolomei, M. S. (1998) · Genes & Development · doi:10.1101/gad.12.23.3693 · Cited by 661
Maternal Obesity Is Associated with Dysregulation of Metabolic, Vascular, and Inflammatory Pathways
Ramsay, J. E., Ferrell, W. R., Crawford, L., Wallace, A. M., Greer, I. A., & Sattar, N. A. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020311 · Cited by 659
Maternal and Fetal Hypothalamic‐Pituitary‐Adrenal Axes During Pregnancy and Postpartum
MASTORAKOS, G., & ILIAS, I. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1290.016 · Cited by 621
Cardiovascular Function Before, During, and After the First and Subsequent Pregnancies
Clapp, J. F., & Capeless, E. L. (1997) · The American Journal of Cardiology · doi:10.1016/s0002-9149(97)00738-8 · Cited by 535
Signalling to translation: How signal transduction pathways control the protein synthetic machinery
Proud, C. G. (2007) · Biochemical Journal · doi:10.1042/bj20070024 · Cited by 520
GSK-3: Functional Insights from Cell Biology and Animal Models
Kaidanovich‐Beilin, O., & Woodgett, J. R. (2011) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2011.00040 · Cited by 505
Placental hormones and the control of maternal metabolism and fetal growth
Newbern, D., & Freemark, M. (2011) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0b013e32834c800d · Cited by 487 · cited 3×
“There is a 60% increase in insulin secretion, which stimulates lipogenesis and reduces fatty acid oxidation, thereby promoting maternal lipid accumulation [8].”
BackgroundInfluential
Regulation of Nutrient Transport across the Placenta
Lager, S., & Powell, T. L. (2012) · Journal of Pregnancy · doi:10.1155/2012/179827 · Cited by 484
Self-citation
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes
Reik, W., Constância, M., Fowden, A. L., Anderson, N. F., Dean, W., Ferguson‐Smith, A. C., Tycko, B., & Sibley, C. P. (2003) · The Journal of Physiology · doi:10.1111/j.1469-7793.2003.00035.x · Cited by 409
The Immunosuppressant Rapamycin Mimics a Starvation-Like Signal Distinct from Amino Acid and Glucose Deprivation
Peng, T., Golub, T. R., & Sabatini, D. M. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.15.5575-5584.2002 · Cited by 404
Modulation of adipokines and cytokines in gestational diabetes and macrosomia
Atègbo, J.-M., Grissa, O., Yessoufou, A., Hichami, A., Dramane, K. L., Moutairou, K., Miled, A., Grissa, A., Jerbi, M., Tabka, Z., et al. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0980 · Cited by 398 · cited 2×
“On the other hand, in obesity and GDM, low maternal adiponectin removes the inhibition of placental insulin signaling, contributing to increased fetal growth (Fig.”
Background
Evidence of Placental Translation Inhibition and Endoplasmic Reticulum Stress in the Etiology of Human Intrauterine Growth Restriction
Yung, H.-W., Calabrese, S., Hynx, D., Hemmings, B. A., Cetin, I., Charnock-Jones, D. S., & Burton, G. J. (2008) · The American Journal of Pathology · doi:10.2353/ajpath.2008.071193 · Cited by 388
The hexosamine signaling pathway: O-GlcNAc cycling in feast or famine
Hanover, J. A., Krause, M., & Love, D. C. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.07.017 · Cited by 352
Parathyroid hormone-related peptide (PTHrP) regulates fetal–placental calcium transport through a receptor distinct from the PTH/PTHrP receptor
Kovács, C. S., Lanske, B., Hunzelman, J. L., Guo, J., Karaplis, A. C., & Kronenberg, H. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.26.15233 · Cited by 347
Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems
Constância, M., Angiolini, E., Sandovici, I., Smith, P., Smith, R., Kelsey, G., Dean, W., Ferguson-Smith, A., Sibley, C. P., Reik, W., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504468103 · Cited by 323 · cited 7×
“Indeed, paternally derived genes are thought to support the extraction of maternal resources for the benefit of a unique offspring, and, on the contrary, maternally derived genes tend to counteract this effect in order to prevent depletion of resources by allocating them equally among different offspring [78, 119].”
BackgroundInfluential
Physiological functions of imprinted genes
Tycko, B., & Morison, I. M. (2002) · Journal of Cellular Physiology · doi:10.1002/jcp.10129 · Cited by 316
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes
Reik, W., Constância, M., Fowden, A. L., et al. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.033274 · Cited by 315
Activation of Placental mTOR Signaling and Amino Acid Transporters in Obese Women Giving Birth to Large Babies
Jansson, N., Rosario, F. J., Gaccioli, F., Lager, S., Jones, H. N., Roos, S., Jansson, T., & Powell, T. L. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2667 · Cited by 305
Self-citation
Maternal Undernutrition Influences Placental-Fetal Development1
Belkacemi, L., Nelson, D. M., Desai, M., & Ross, M. G. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.110.084517 · Cited by 299
Association between the Activity of the System A Amino Acid Transporter in the Microvillous Plasma Membrane of the Human Placenta and Severity of Fetal Compromise in Intrauterine Growth Restriction
Glazier, J. D., Cetin, I., Perugino, G., Ronzoni, S., Grey, A. M., Mahendran, D., Marconi, A. M., Pardi, G., & Sibley, C. P. (1997) · Pediatric Research · doi:10.1203/00006450-199710000-00016 · Cited by 287
Mammalian target of rapamycin in the human placenta regulates leucine transport and is down‐regulated in restricted fetal growth
Roos, S., Jansson, N., Palmberg, I., Säljö, K., Powell, T. L., & Jansson, T. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.129676 · Cited by 283
Self-citation
Placental structure and inflammation in pregnancies associated with obesity
Roberts, K., Riley, S. C., Reynolds, R. M., Barr, S., Evans, M., Statham, A., Hor, K., Jabbour, H. N., Norman, J. E., & Denison, F. C. (2011) · Placenta · doi:10.1016/j.placenta.2010.12.023 · Cited by 281
Longitudinal changes in maternal serum leptin concentrations, body composition, and resting metabolic rate in pregnancy
Highman, T. J., Friedman, J. E., Huston, L. P., Wong, W. W., & Catalano, P. M. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70540-x · Cited by 277
Adiponectin in human pregnancy: implications for regulation of glucose and lipid metabolism
Catalano, P. M., Hoegh, A. M., Minium, J., Huston-Presley, L., Bernard, S. L., Kalhan, S. C., & Mouzon, S. H. (2006) · Diabetologia · doi:10.1007/s00125-006-0264-x · Cited by 275
Down‐regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet
Jansson, N., Pettersson, J., Haafiz, A., Ericsson, A., Palmberg, I., Tranberg, M., Ganapathy, V., Powell, T. L., & Jansson, T. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.550004 · Cited by 265
Self-citation
Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet
Jansson, N., Pettersson, J., Haafiz, A., Ericsson, A., Palmberg, I., Tranberg, M., Ganapathy, V., Powell, T. L., & Jansson, T. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.116509 · Cited by 261
Self-citation
Umbilical amino acid concentrations in normal and growth-retarded fetuses sampled in utero by cordocentesis
Cetin, I., Corbetta, C., Sereni, L. P., Marconi, A. M., Bozzetti, P., Pardi, G., & Battaglia, F. C. (1990) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(90)90860-a · Cited by 259
Human Placental Transport in Altered Fetal Growth: Does the Placenta Function as a Nutrient Sensor? – A Review
Jansson, T., & Powell, T. L. (2006) · Placenta · doi:10.1016/j.placenta.2005.11.010 · Cited by 257
Self-citation
Amino Acid Transporters in the Human Placenta
Jansson, T. (2001) · Pediatric Research · doi:10.1203/00006450-200102000-00003 · Cited by 245
Self-citation
Leptin Stimulates the Activity of the System A Amino Acid Transporter in Human Placental Villous Fragments
Jansson, N., Greenwood, S. L., Johansson, B. R., Powell, T. L., & Jansson, T. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021332 · Cited by 243
Self-citation
Alterations in the Activity of Placental Amino Acid Transporters in Pregnancies Complicated by Diabetes
Jansson, T., Ekstrand, Y., Björn, C., Wennergren, M., & Powell, T. L. (2002) · Diabetes · doi:10.2337/diabetes.51.7.2214 · Cited by 238
Self-citation
Imprinted genes in the placenta – A review
Coan, P. M., Burton, G. J., & Ferguson‐Smith, A. C. (2005) · Placenta · doi:10.1016/j.placenta.2004.12.009 · Cited by 238
Placental Transport of Leucine and Lysine Is Reduced in Intrauterine Growth Restriction1
Jansson, T., Scholtbach, V., & Powell, T. L. (1998) · Pediatric Research · doi:10.1203/00006450-199810000-00011 · Cited by 235
Self-citation
The H19 gene: regulation and function of a non-coding RNA
Gabory, A., Ripoche, M., Yoshimizu, T., & Dandolo, L. (2006) · Cytogenetic and Genome Research · doi:10.1159/000090831 · Cited by 227
Maternal vasodilation in pregnancy: the emerging role of relaxin
Conrad, K. P. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00156.2011 · Cited by 222
Maternal blood volume and cardiac output during pregnancy: a hypothesis of endocrinologic control
Longo, L. D. (1983) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1983.245.5.r720 · Cited by 221
Glucose Transport and System A Activity in Syncytiotrophoblast Microvillous and Basal Plasma Membranes in Intrauterine Growth Restriction
Jansson, T., Ylvén, K., Wennergren, M., & Powell, T. L. (2002) · Placenta · doi:10.1053/plac.2002.0826 · Cited by 218
Self-citation
Human placental growth hormone causes severe insulin resistance in transgenic mice
Barbour, L. A., Shao, J., Qiao, L., Pulawa, L. K., Jensen, D. R., Bartke, A., Garrity, M., Draznin, B., & Friedman, J. E. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.121256 · Cited by 214
Blood glucose and oxygen tension levels in small-for-gestational-age fetuses
Economides, D. L., & Nicolaides, K. H. (1989) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(89)90453-5 · Cited by 208
Human Placental Growth Hormone Increases Expression of the P85 Regulatory Unit of Phosphatidylinositol 3-Kinase and Triggers Severe Insulin Resistance in Skeletal Muscle
Barbour, L. A., Shao, J., Qiao, L., Leitner, W., Anderson, M., Friedman, J. E., & Draznin, B. (2004) · Endocrinology · doi:10.1210/en.2003-1297 · Cited by 208
Placental growth hormone levels in normal pregnancy and in pregnancies with intrauterine growth retardation
Mirlesse, V., Frankenne, F., Alsat, E., Poncelet, M., Hennen, G., & Evain-Brion, D. (1993) · Pediatric Research · doi:10.1203/00006450-199310000-00011 · Cited by 202
Adiponectin in Human Cord Blood: Relation to Fetal Birth Weight and Gender
Sivan, E., Mazaki‐Tovi, S., Pariente, C., Efraty, Y., Schiff, E., Hemi, R., & Kanety, H. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031174 · Cited by 202
Placental nutrient supply and fetal growth
Desforges, M., & Sibley, C. P. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082765md · Cited by 199
Glycogen Synthase Kinase 3α and 3β Mediate a Glucose-Sensitive Antiapoptotic Signaling Pathway To Stabilize Mcl-1
Zhao, Y., Altman, B. J., Coloff, J. L., Herman, C. E., Jacobs, S. R., Wieman, H. L., Wofford, J. A., DiMascio, L. N., Ilkayeva, O., Kelekar, A., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00153-07 · Cited by 195
Mammalian target of rapamycin signalling modulates amino acid uptake by regulating transporter cell surface abundance in primary human trophoblast cells
Rosario, F. J., Kanai, Y., Powell, T. L., & Jansson, T. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.238014 · Cited by 185
Self-citation
Cord Blood Leptin and Insulin-Like Growth Factor Levels are Independent Predictors of Fetal Growth
Christou, H. A., Connors, J. M., Ziotopoulou, M., Hatzidakis, V., Papathanassoglou, E. D. E., Ringer, S. A., & Mantzoros, C. S. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.2.7217 · Cited by 185
Review: The placenta and developmental programming: Balancing fetal nutrient demands with maternal resource allocation
Burton, G. J., & Fowden, A. L. (2012) · Placenta · doi:10.1016/j.placenta.2011.11.013 · Cited by 177
Inflammatory Mediators and Glucose in Pregnancy: Results from a Subset of the Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study
Lowe, L. P., Metzger, B. E., Lowe, W. L., Dyer, A. R., McDade, T. W., & McIntyre, D. H. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1662 · Cited by 177
Human Placental Growth Hormone—A Review
Lacroix, M. C., Guibourdenche, J., Frendo, J., MULLER, F. M., & Evain‐Brion, D. (2002) · Placenta · doi:10.1053/plac.2002.0811 · Cited by 177
Maternal Protein Restriction in the Rat Inhibits Placental Insulin, mTOR, and STAT3 Signaling and Down-Regulates Placental Amino Acid Transporters
Rosario, F. J., Jansson, N., Kanai, Y., Prasad, P. D., Powell, T. L., & Jansson, T. (2011) · Endocrinology · doi:10.1210/en.2010-1153 · Cited by 176
Self-citation
The emerging role of mTORC1 signaling in placental nutrient-sensing
Jansson, T., Aye, I. L. M. H., & Goberdhan, D. C. I. (2012) · Placenta · doi:10.1016/j.placenta.2012.05.010 · Cited by 175
Self-citation
Role of placental nutrient sensing in developmental programming
JANSSON, T., & POWELL, T. L. (2013) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3182993a2e · Cited by 172
Self-citation
IL-6 stimulates system A amino acid transporter activity in trophoblast cells through STAT3 and increased expression of SNAT2
Jones, H. N., Jansson, T., & Powell, T. L. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00195.2009 · Cited by 168 · cited 2×
“Moreover, the activation of trophoblast system A activity by IL-6, leptin, and oleic acid appears to involve the transcription factor STAT-3 [49, 52, 53], indicating that there are common pathways to integrate and ‘‘sense’’ different maternal metabolic cues.”
BackgroundSelf-citation
Regulation of amino acid transporters by glucose and growth factors in cultured primary human trophoblast cells is mediated by mTOR signaling
Roos, S., Lagerlöf, O., Wennergren, M., Powell, T. L., & Jansson, T. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00191.2009 · Cited by 168
Self-citation
Control of vascular resistance in the human placenta
Myatt, L. (1992) · Placenta · doi:10.1016/0143-4004(92)90057-z · Cited by 164
Maternal hormones linking maternal body mass index and dietary intake to birth weight
Jansson, N., Nilsfelt, A., Gellerstedt, M., Wennergren, M., Rossander-Hulthén, L., Powell, T. L., & Jansson, T. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.6.1743 · Cited by 159
Self-citation
Review: Adiponectin – The missing link between maternal adiposity, placental transport and fetal growth?
Aye, I. L. M. H., Powell, T. L., & Jansson, T. (2012) · Placenta · doi:10.1016/j.placenta.2012.11.024 · Cited by 158
Self-citation
The Mechanisms and Regulation of Placental Amino Acid Transport to the Human Foetus
Cleal, J. K., & Lewis, R. M. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01662.x · Cited by 157
Intrauterine Growth Restriction in Humans Is Associated with Abnormalities in Placental Insulin-Like Growth Factor Signaling
Laviola, L., Perrini, S., Belsanti, G., Natalicchio, A., Montrone, C., Leonardini, A., Vimercati, A., Scioscia, M., Selvaggi, L. E., GIORGINO, R., et al. (2004) · Endocrinology · doi:10.1210/en.2004-1332 · Cited by 151
Regulation of placental amino acid transporter activity by mammalian target of rapamycin
Roos, S., Kanai, Y., Prasad, P. D., Powell, T. L., & Jansson, T. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00330.2008 · Cited by 150
Self-citation
Effect of low-protein diet-induced intrauterine growth retardation on rat placental amino acid transport
Malandro, M. S., Beveridge, M. J., Kilberg, M. S., & Novak, D. (1996) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1996.271.1.c295 · Cited by 150
Plasma catecholamine responses to physiologic stimuli in normal human pregnancy
Barron, W. M., MUJAIS, S. K., Zinaman, M. J., Bravo, E. L., & Lindheimer, M. D. (1986) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(86)90397-2 · Cited by 148
The Transcription Factor Network Associated With the Amino Acid Response in Mammalian Cells
Kilberg, M. S., Balasubramanian, M. N., Fu, L., & Shan, J. (2012) · Advances in Nutrition · doi:10.3945/an.112.001891 · Cited by 144
Maternal obesity markedly increases placental fatty acid transporter expression and fetal blood triglycerides at midgestation in the ewe
Zhu, M. J., Ma, Y., Long, N. M., Du, M., & Ford, S. P. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00309.2010 · Cited by 137
Full-Length Adiponectin Attenuates Insulin Signaling and Inhibits Insulin-Stimulated Amino Acid Transport in Human Primary Trophoblast Cells
Jones, H. N., Jansson, T., & Powell, T. L. (2010) · Diabetes · doi:10.2337/db09-0824 · Cited by 136
Self-citation
Down‐regulation of placental mTOR, insulin/IGF‐I signaling, and nutrient transporters in response to maternal nutrient restriction in the baboon
Kavitha, J., Rosario, F. J., Nijland, M. J., McDonald, T. J., Wu, G., Kanai, Y., Powell, T. L., Nathanielsz, P. W., & Jansson, T. (2013) · The FASEB Journal · doi:10.1096/fj.13-242271 · Cited by 135
Self-citation
An obesogenic diet during mouse pregnancy modifies maternal nutrient partitioning and the fetal growth trajectory
Sferruzzi‐Perri, A. N., Vaughan, O. R., Haro, M., Cooper, W. N., Musial, B., Charalambous, M., Pestana, D., Ayyar, S., Ferguson‐Smith, A. C., Burton, G. J., et al. (2013) · The FASEB Journal · doi:10.1096/fj.13-234823 · Cited by 134
Maternal serum adiponectin levels during human pregnancy
Mazaki‐Tovi, S., Kanety, H., Pariente, C., Hemi, R., Wiser, A., Schiff, E., & Sivan, E. (2007) · Journal of Perinatology · doi:10.1038/sj.jp.7211639 · Cited by 130
Placental transport in response to altered maternal nutrition
Gaccioli, F., Lager, S., Powell, T. L., & Jansson, T. (2013) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174412000529 · Cited by 129
Self-citation
Characterisation of L‐tryptophan transporters in human placenta: a comparison of brush border and basal membrane vesicles
Kudo, Y., & Boyd, C. A. R. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0405i.x · Cited by 121
Regulation of Maternal Metabolism by Pituitary and Placental Hormones: Roles in Fetal Development and Metabolic Programming
Freemark, M. (2006) · Hormone Research in Paediatrics · doi:10.1159/000091505 · Cited by 118
Placental-Specific Igf2 Deficiency Alters Developmental Adaptations to Undernutrition in Mice
Sferruzzi-Perri, A. N., Vaughan, O. R., Coan, P. M., Suciu, M. C., Darbyshire, R., Constancia, M., Burton, G. J., & Fowden, A. L. (2011) · Endocrinology · doi:10.1210/en.2011-0240 · Cited by 115
Maternal-fetal resource allocation: Co-operation and conflict
Fowden, A. L., & Moore, T. (2012) · Placenta · doi:10.1016/j.placenta.2012.05.002 · Cited by 114
Insulin‐like growth factor‐1 stimulates amino acid uptake by the cultured human placental trophoblast
Karl, P. I. (1995) · Journal of Cellular Physiology · doi:10.1002/jcp.1041650111 · Cited by 112
Evidence of endoplasmic reticulum stress and protein synthesis inhibition in the placenta of non‐native women at high altitude
Yung, H. W., Cox, M., van Patot, M. T., & Burton, G. J. (2012) · The FASEB Journal · doi:10.1096/fj.11-190082 · Cited by 112
Altered activity of the system A amino acid transporter in microvillous membrane vesicles from placentas of macrosomic babies born to diabetic women.
Kuruvilla, A. G., D'Souza, S. W., Glazier, J. D., Mahendran, D., Maresh, M., & Sibley, C. P. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117386 · Cited by 107
Chronic maternal infusion of full‐length adiponectin in pregnant mice down‐regulates placental amino acid transporter activity and expression and decreases fetal growth
Rosario, F. J., Schumacher, M. A., Jiang, J. X., Kanai, Y., Powell, T. L., & Jansson, T. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.226399 · Cited by 104
Self-citation
Interleukin-1β inhibits insulin signaling and prevents insulin-stimulated system A amino acid transport in primary human trophoblasts
Aye, I. L. M. H., Jansson, T., & Powell, T. L. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.07.013 · Cited by 96
Self-citation
Review: Adaptation in placental nutrient supply to meet fetal growth demand: Implications for programming
Sibley, C. P., Brownbill, P., Dilworth, M. R., & Glazier, J. D. (2010) · Placenta · doi:10.1016/j.placenta.2009.12.020 · Cited by 95
Insulin receptors in syncytitrophoblast and fetal endothelium of human placenta. Immunohistochemical evidence for developmental changes in distribution pattern
Desoyé, G., Hahn, T., Hartmann, M., Blaschitz, A., Dohr, G., Kohnen, G., & Kaufmann, P. (1994) · Histochemistry and Cell Biology · doi:10.1007/bf00315915 · Cited by 93
Neutral Amino Acid Uptake by the Microvillous Plasma Membrane of the Human Placenta Is Inversely Related to Fetal Size at Birth in Normal Pregnancy1
Godfrey, K. M., Matthews, N., Glazier, J. D., Jackson, A. A., Wilman, C., & Sibley, C. P. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.9.5132 · Cited by 85
Placental-specific Igf2 knockout mice exhibit hypocalcemia and adaptive changes in placental calcium transport
Dilworth, M., Kusinski, L. C., Cowley, E. J., Ward, B. S., Husain, S. M., Constância, M., Sibley, C. P., & Glazier, J. D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911710107 · Cited by 85
Leptin Receptor in Human Term Placenta: in Situ Hybridization and Immunohistochemical Localization
Bodner, J., Ebenbichler, C. F., Wolf, H. J., Müller‐Holzner, E., Stanzl, U., Gander, R., Huter, O., & Patsch, J. R. (1999) · Placenta · doi:10.1053/plac.1999.0431 · Cited by 84
Expression and regulation of 4F2hc and hLAT1 in human trophoblasts
Okamoto, Y., Sakata, M., Ogura, K., Yamamoto, T., Yamaguchi, M., Tasaka, K., Kurachi, H., Tsurudome, M., & Murata, Y. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2002.282.1.c196 · Cited by 79
Estrogen Receptor-α and Estrogen Receptor-β in the Uterine Vascular Endothelium during Pregnancy: Functional Implications for Regulating Uterine Blood Flow
Pastore, M. B., Jobe, S. O., Ramadoss, J., & Magness, R. R. (2012) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1299597 · Cited by 77
Maternal amino acid supplementation for intrauterine growth restriction
Rozance, P. J. (2010) · Frontiers in Bioscience-Scholar · doi:10.2741/s162 · Cited by 77
Maternal Overweight Induced by a Diet with High Content of Saturated Fat Activates Placental mTOR and eIF2alpha Signaling and Increases Fetal Growth in Rats1
Gaccioli, F., White, V., Capobianco, E., Powell, T. L., Jawerbaum, A., & Jansson, T. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.113.109702 · Cited by 76
Self-citation
Adiponectin Inhibits Insulin Function in Primary Trophoblasts by PPARα-Mediated Ceramide Synthesis
Aye, I. L. M. H., Gao, X., Weintraub, S. T., Jansson, T., & Powell, T. L. (2014) · Molecular Endocrinology · doi:10.1210/me.2013-1401 · Cited by 75
Self-citation
Maternal corticosterone regulates nutrient allocation to fetal growth in mice
Vaughan, O. R., Sferruzzi‐Perri, A. N., & Fowden, A. L. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.239426 · Cited by 75
Distinct Actions of Insulin-Like Growth Factors (IGFs) on Placental Development and Fetal Growth: Lessons from Mice and Guinea Pigs
Roberts, C. T., Owens, J. A., & Sferruzzi-Perri, A. N. (2008) · Placenta · doi:10.1016/j.placenta.2007.12.002 · Cited by 74
Neutral Amino Acid Uptake by the Microvillous Plasma Membrane of the Human Placenta Is Inversely Related to Fetal Size at Birth in Normal Pregnancy
Godfrey, K. M. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.9.3320 · Cited by 72
Leptin Affects System A Amino Acid Transport Activity in the Human Placenta: Evidence for STAT3 Dependent Mechanisms
von Versen‐Höynck, F., Rajakumar, A., Parrott, M. S., & Powers, R. W. (2009) · Placenta · doi:10.1016/j.placenta.2009.01.004 · Cited by 71
Human placental amino acid transporter genes: expression and function
Kudo, Y., & Boyd, C. A. R. (2002) · Reproduction · doi:10.1530/rep.0.1240593 · Cited by 71
Fetal amino acids in normal pregnancies and in pregnancies complicated by intrauterine growth retardation
Cetin, I., Marconi, A. M., Corbetta, C., Lanfranchi, A. K., Baggiani, A., Battaglia, F. C., & Pardi, G. (1992) · Early Human Development · doi:10.1016/0378-3782(92)90136-5 · Cited by 70
Developmental adaptations to increased fetal nutrient demand in mouse genetic models of Igf2‐mediated overgrowth
Angiolini, E., Coan, P. M., Sandovici, I., Iwajomo, O. H., Peck, G., Burton, G. J., Sibley, C. P., Reik, W., Fowden, A. L., & Constância, M. (2011) · The FASEB Journal · doi:10.1096/fj.10-175273 · Cited by 64
Oleic acid stimulates system A amino acid transport in primary human trophoblast cells mediated by toll-like receptor 4
Lager, S., Gaccioli, F., Ramirez, V. I., Jones, H. N., Jansson, T., & Powell, T. L. (2012) · Journal of Lipid Research · doi:10.1194/jlr.m033050 · Cited by 61
Self-citation
Increased maternofetal calcium flux in parathyroid hormone‐related protein‐null mice
Bond, H., Dilworth, M. R., Baker, B., Cowley, E. J., Jimenez, A. R., Boyd, R. D. H., Husain, S. M., Ward, B. S., Sibley, C. P., & Glazier, J. D. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.149104 · Cited by 60
ATP Dependent Ca2+ Transport Across Basal Membrane of Human Syncytiotrophoblast in Pregnancies Complicated by Intrauterine Growth Restriction or Diabetes
Strid, H., Bucht, E., Jansson, T., Wennergren, M., & Powell, T. L. (2003) · Placenta · doi:10.1053/plac.2002.0941 · Cited by 60
Self-citation
Vasorelaxant action of 17β-estradiol in rat uterine arteries: role of nitric oxide synthases and estrogen receptors
Scott, P.-A., Tremblay, A., Brochu, M., & St‐Louis, J. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00736.2007 · Cited by 59
Human uterine and placental arteries exhibit tissue-specific acute responses to 17 -estradiol and estrogen-receptor-specific agonists
Corcoran, J. J., Nicholson, C., Sweeney, M., Charnock, J. C., Robson, S. C., Westwood, M., & Taggart, M. J. (2013) · Molecular Human Reproduction · doi:10.1093/molehr/gat095 · Cited by 59
Upregulation of growth signaling and nutrient transporters in cotyledons of early to mid-gestational nutrient restricted ewes
Ma, Y., Zhu, M. J., Uthlaut, A. B., Nijland, M. J., Nathanielsz, P. W., Hess, B. W., & Ford, S. P. (2011) · Placenta · doi:10.1016/j.placenta.2011.01.007 · Cited by 58 · cited 1×
“Placental AMPK phosphorylation has been reported to be increased in sheep subjected to 50% calorie restriction [100] and decreased in overnourished, obese pregnant ewes [101], high-fat diet-fed pregnant rats [97], and obese women giving birth to large babies [89].”
Background
Spatial Polarization of Insulin-Like Growth Factor Receptors on the Human Syncytiotrophoblast
Fang, J., Furesz, T. C., Laurent, R. S., Smith, C. H., & Fant, M. E. (1997) · Pediatric Research · doi:10.1203/00006450-199702000-00017 · Cited by 55
Adiponectin Enhances Mouse Fetal Fat Deposition
Qiao, L., Yoo, H. S., Madon, A., Kinney, B., Hay, W. W., & Shao, J. (2012) · Diabetes · doi:10.2337/db12-0055 · Cited by 55
Down-Regulation of Growth Signaling Pathways Linked to a Reduced Cotyledonary Vascularity in Placentomes of Over-Nourished, Obese Pregnant Ewes
Zhu, M. J., Du, M., Nijland, M. J., Nathanielsz, P. W., Hess, B. W., Moss, G. E., & Ford, S. P. (2009) · Placenta · doi:10.1016/j.placenta.2009.02.001 · Cited by 54
Impairment of insulin receptor signal transduction in placentas of intra-uterine growth-restricted newborns and its relationship with fetal growth
Street, M. E., Viani, I., Ziveri, M. A., Volta, C., Smerieri, A., & Bernasconi, S. (2010) · European Journal of Endocrinology · doi:10.1530/eje-10-0752 · Cited by 51
Placental mammalian target of rapamycin and related signaling pathways in an ovine model of intrauterine growth restriction
Arroyo, J. A., Brown, L. D., & Galan, H. L. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.07.031 · Cited by 47
Antenatal Dexamethasone Treatment in Midgestation Reduces System A-Mediated Transport in the Late-Gestation Murine Placenta
Audette, M. C., Challis, J. R. G., Jones, R. L., Sibley, C. P., & Matthews, S. G. (2011) · Endocrinology · doi:10.1210/en.2011-0104 · Cited by 47
Effects of Cord Serum Insulin, IGF-II, IGFBP-2, IL-6 and Cortisol Concentrations on Human Birth Weight and Length: Pilot Study
Smerieri, A., Petraroli, M., Ziveri, M. A., Volta, C., Bernasconi, S., & Street, M. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029562 · Cited by 46
Parathyroid hormone-related peptide (38-94) amide stimulates ATP-dependent calcium transport in the Basal plasma membrane of the human syncytiotrophoblast
Strid, H., Care, A. D., Jansson, T., & Powell, T. L. (2002) · Journal of Endocrinology · doi:10.1677/joe.0.1750517 · Cited by 43
Self-citation
Periconceptional Nutrient Restriction in the Ewe Alters MAPK/ERK1/2 and PI3K/Akt Growth Signaling Pathways and Vascularity in the Placentome
Zhu, M. J., Du, M., Hess, B. W., Nathanielsz, P. W., & Ford, S. P. (2007) · Placenta · doi:10.1016/j.placenta.2007.05.004 · Cited by 41
A Low-Protein Diet during Gestation in Rats Activates the Placental Mammalian Amino Acid Response Pathway and Programs the Growth Capacity of Offspring
Strakovsky, R. S., Zhou, D., & Pan, Y. (2010) · Journal of Nutrition · doi:10.3945/jn.110.127803 · Cited by 40
Placental growth hormone levels in normal pregnancy and in pregnancies with intrauterine growth retardation
Alsat, E., Mirlesse, V., Frankenne, F., Poncelet, M., Hennen, G. P., & Evain‐Brion, D. (1993) · Placenta · doi:10.1016/s0143-4004(05)80469-2 · Cited by 34
Differential expression of the receptors for epidermal growth factor and insulin in the developing human placenta
Tavaré, J. M., & Holmes, C. H. (1989) · Cellular Signalling · doi:10.1016/0898-6568(89)90020-x · Cited by 32
Altitude and fetal growth: current knowledge and future directions
Zamudio, S., & MOORE, L. G. (2000) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2000.00155.x · Cited by 28
IGF regulation of neutral amino acid transport in the BeWo choriocarcinoma cell line (b30 clone): Evidence for MAP kinase-dependent and MAP kinase-independent mechanisms
Fang, J., Mao, D., Smith, C. H., & Fant, M. E. (2006) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2006.08.002 · Cited by 28
The Ultrastructural Basis of the Nutritional Transfer: Evidence of Different Patterns in the Plasma Membranes of the Multilayered Placental Barrier
Sideri, M. G., de Virgiliis, G., Rainoldi, R., & Remotti, G. (1984) · Springer eBooks · doi:10.1007/978-1-4684-1191-1_3 · Cited by 22
l-Methionine Placental Uptake: Characterization and Modulation in Gestational Diabetes Mellitus
Araújo, J. R., Correia‐Branco, A., Ramalho, C. M. A., Gonçalves, P., Pinho, M. J., Keating, E., & Martel, F. (2013) · Reproductive Sciences · doi:10.1177/1933719113488442 · Cited by 21
IFPA Meeting 2011 workshop report I: Placenta: Predicting future health; roles of lipids in the growth and development of feto-placental unit; placental nutrient sensing; placental research to solve clinical problems – A translational approach
Acharya, G., Albrecht, C., Benton, S. J., Cotechini, T., Dechend, R., Dilworth, M. R., Duttaroy, A. K., Grotmol, T., Heazell, A. E. P., Jansson, T., et al. (2011) · Placenta · doi:10.1016/j.placenta.2011.11.015 · Cited by 9
Self-citation
The hypoxia of high altitude causes restricted fetal growth in chick embryos with the extent of this effect depending on maternal altitudinal status
Mehta, A. R., & Mehta, P. R. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.151332 · Cited by 6

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Authors: Díaz, P., Powell, T. L., & Jansson, T.
Affiliations: The University of Texas at San Antonio Health Science Center (US)
Corresponding author: Díaz, Paula
ORCID: Díaz, Paula
Powell, Theresa L.
Jansson, Thomas
Venue: Biology of Reproduction
Publisher: Oxford University Press (OUP)
Published: 2014-10-01
Volume: 91
Issue: 4
Pages: 82-82
ISSN: 0006-3363 (ISSN-L)
1529-7268
DOI: 10.1095/biolreprod.114.121798
PMC: PMC4435028
OpenAlex: W2151264384
Cited by: 158
References: 128
Citations by year: 2026: 19 · 2025: 16 · 2024: 11 · 2023: 18 · 2022: 11 · 2021: 14 · 2020: 8 · 2019: 12 · 2018: 12 · 2017: 15 · 2016: 9 · 2015: 12 · 2014: 1
FWCI: 1.86
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Biology of Reproduction (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
BioOne Complete (BioOne) (submittedVersion)
Funders: National Institutes of Health (5r01hd068370-11, HD065007, HD068370)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK089989, DK089989)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD071306, R01-HD068370, HD065007, R01HD065007, HD071306, HD 068370)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
Keywords: placental development, nutrient transporters, maternal-fetal nutrient exchange, maternal undernutrition, maternal overnutrition, maternal obesity, gestational diabetes mellitus, fetal programming, evolutionary pressure, placenta
MeSH terms: Animals, Biological Transport, Female, Maternal-Fetal Exchange, Placenta, Pregnancy, Prenatal Nutritional Physiological Phenomena

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The Role of Placental Nutrient Sensing in Maternal-Fetal Resource Allocation1

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