Human Placental Growth Hormone Increases Expression of the P85 Regulatory Unit of Phosphatidylinositol 3-Kinase and Triggers Severe Insulin Resistance in Skeletal Muscle
Abstract
The insulin resistance of normal pregnancy is necessary to divert fuels to the fetus to meet fetal growth demands and is mediated by placental hormones. We recently demonstrated that human placental GH (hPGH) can trigger severe insulin resistance in transgenic (TG) mice. In this study we sought to elucidate the cellular mechanisms by which hPGH interferes with insulin signaling in muscle in TG mice. Insulin-stimulated GLUT-4 translocation to the plasma membrane (PM) was reduced in the TG compared with wild-type (WT) mice (P = 0.05). Insulin receptor (IR) levels were modestly reduced by 19% (P < 0.01) in TG mice, but there were no changes in phosphorylation of IR or IR substrate-1 (IRS-1) between WT and TG mice. A singular finding was a highly significant increase in the p85α regulatory subunit of phosphatidylinositol 3-kinase (PI 3-kinase; P < 0.001), yet a reduced ability of insulin to stimulate IRS-1-associated PI 3-kinase activity (P < 0.05). Although the levels of the p110 catalytic subunit protein of PI 3-kinase and IRS-1 were unchanged in the TG mice, insulin’s ability to stimulate p110 association with IRS-1 was markedly reduced (P < 0.0001). We demonstrate a unique mechanism of insulin resistance and suggest that hPGH may contribute to the insulin resistance of normal pregnancy by increasing the expression of the p85α monomer, which competes in a dominant negative fashion with the p85-p110 heterodimer for binding to IRS-1 protein.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Later in pregnancy, a state of insulin resistance develops in peripheral maternal tissues, mediated in part through the actions of placental growth hormone.
“Later in pregnancy, a state of insulin resistance develops in the peripheral maternal tissues, mediated, in part, through the actions of placental growth hormone (23).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [23]
Cites
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 · see citing works
Self-citationInsulin regulation of glucose uptake: a complex interplay of intracellular signalling pathways
A., K., & J., P. (2002) · Diabetologia · doi:10.1007/s00125-002-0974-7 · Cited by 438 · see citing works
Brelje, T. C., Scharp, D. W., Lacy, P. E., Ogren, L., Talamantes, F. J., Robertson, M. C., Friesen, H. G., & Sorenson, R. L. (1993) · Endocrinology · doi:10.1210/endo.132.2.8425500 · Cited by 409 · see citing works
Terauchi, Y., Tsuji, Y., Satoh, S., Minoura, H., Murakami, K., Okuno, A., Inukai, K., Asano, T., Kaburagi, Y., Ueki, K., et al. (1999) · Nature Genetics · doi:10.1038/6023 · Cited by 399 · see citing works
Handwerger, S., & Freemark, M. (2000) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem.2000.13.4.343 · Cited by 351 · see citing works
Recent Advances in Our Understanding of Insulin Action and Insulin Resistance
Roith, D. L., & Zick, Y. (2001) · Diabetes Care · doi:10.2337/diacare.24.3.588 · Cited by 337 · see citing works
Kerouz, N., Hörsch, D., Pons, S., & Kahn, C. R. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119872 · Cited by 301 · see citing works
Friedman, J. E., Ishizuka, T., Shao, J., Huston, L., Highman, T., & Catalano, P. (1999) · Diabetes · doi:10.2337/diabetes.48.9.1807 · Cited by 255 · see citing works
Self-citationMauvais‐Jarvis, F., Ueki, K., Fruman, D. A., Hirshman, M. F., Sakamoto, K., Goodyear, L. J., Iannacone, M., Accili, D., Cantley, L. C., & Kahn, C. R. (2002) · Journal of Clinical Investigation · doi:10.1172/jci13305 · Cited by 245 · see citing works
Growth Hormone (GH), GH Receptor, and Signal Transduction
Kopchick, J. J., & Andry, J. M. (2000) · Molecular Genetics and Metabolism · doi:10.1006/mgme.2000.3068 · Cited by 233 · see citing works
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 · see citing works
Self-citationMauvais-Jarvis, F., Ueki, K., Fruman, D. A., Hirshman, M. F., Sakamoto, K., Goodyear, L. J., Iannacone, M., Accili, D., Cantley, L. C., & Kahn, C. R. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0213305 · Cited by 207 · see citing works
Ueki, K., Algenstaedt, P., Mauvais-Jarvis, F., & Kahn, C. R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.21.8035-8046.2000 · Cited by 148 · see citing works
Physiological role of human placental growth hormone
Alsat, E., Guibourdenche, J., Couturier, A., & Evain‐Brion, D. (1998) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(98)00040-9 · Cited by 136 · see citing works
Sakaue, H., Ogawa, W., Takata, M., Kuroda, S., Kotani, K., Matsumoto, M., Sakaue, M., Nishio, S., Ueno, H., & Kasuga, M. (1997) · Molecular Endocrinology · doi:10.1210/mend.11.10.9986 · Cited by 125 · see citing works
Takano, A., Haruta, T., Iwata, M., Usui, I., Uno, T., Kawahara, J., Ueno, E., Sasaoka, T., & Kobayashi, M. (2001) · Diabetes · doi:10.2337/diabetes.50.8.1891 · Cited by 110 · see citing works
Shao, J., Catalano, P. M., Yamashita, H., Ruyter, I., Smith, S. R., YOUNGREN, J. F., & Friedman, J. E. (2000) · Diabetes · doi:10.2337/diabetes.49.4.603 · Cited by 108 · see citing works
Self-citationGrowth Hormone-Induced Alterations in the Insulin-Signaling System
Dominici, F. P., & Turyn, D. (2002) · Experimental Biology and Medicine · doi:10.1177/153537020222700301 · Cited by 105 · see citing works
Dominici, F. P., Cifone, D., Bartke, A., & Turyn, D. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.277.3.e447 · Cited by 70 · see citing works
Shao, J., Yamashita, H., Qiao, L., Draznin, B., & Friedman, J. E. (2002) · Diabetes · doi:10.2337/diabetes.51.1.19 · Cited by 69 · see citing works
Self-citationYamashita, H., Shao, J., & Friedman, J. E. (2000) · Clinical Obstetrics & Gynecology · doi:10.1097/00003081-200003000-00009 · Cited by 68 · see citing works
Self-citationZhang, B. B. (2002) · Frontiers in bioscience · doi:10.2741/a820 · Cited by 47 · see citing works
Expression of the human growth hormone variant gene in cultured fibroblasts and transgenic mice.
Selden, R. F., Wagner, T. E., Blethen, S. L., Yun, J. S., Rowe, M. E., & Goodman, H. M. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.21.8241 · Cited by 46 · see citing works
Jiang, G. (2002) · Frontiers in bioscience · doi:10.2741/jiang · Cited by 42 · see citing works
Placental Lactogen and Growth Hormone
Anthony, R. V., Limesand, S. W., Fanning, M. D., & Liang, R. (1998) · Humana Press eBooks · doi:10.1007/978-1-4612-1804-3_16 · Cited by 38 · see citing works
Placental growth hormone variant: assay and clinical aspects
Evain‐Brion, D., Alsat, E., Igout, A., Frankenne, F., & Hennen, G. P. (1994) · Acta Paediatrica · doi:10.1111/j.1651-2227.1994.tb13287.x · Cited by 35 · see citing works
Eriksson, H., Ridderstråle, M., & Tornqvist, H. E. (1995) · Endocrinology · doi:10.1210/endo.136.11.7588246 · Cited by 23 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism
Engelman, J. A., Luo, J., & Cantley, L. C. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1879 · Cited by 3,330 · see citing works
Critical nodes in signalling pathways: insights into insulin action
Taniguchi, C. M., Emanuelli, B., & Kahn, C. R. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1837 · Cited by 2,760 · see citing works
PI3K/AKT/mTOR signaling transduction pathway and targeted therapies in cancer
Glaviano, A., Foo, A. S. C., Lam, H. Y., Yap, K. C. H., Jacot, W., Jones, R. H., Eng, H., Nair, M. G., Makvandi, P., Geoerger, B., et al. (2023) · Molecular Cancer · doi:10.1186/s12943-023-01827-6 · Cited by 2,138 · see citing works
The Placenta: A Multifaceted, Transient Organ
Burton, G. J., & Fowden, A. L. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0066 · Cited by 833 · see citing works
Regulation of glucose homeostasis by glucocorticoids
Kuo, T., McQueen, A., Chen, T.-C., & Wang, J.-C. (2015) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-2895-8_5 · Cited by 723 · see citing works
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
FROM MICE TO MEN: Insights into the Insulin Resistance Syndromes
Biddinger, S. B., & Kahn, C. R. (2005) · Annual Review of Physiology · doi:10.1146/annurev.physiol.68.040104.124723 · Cited by 700 · see citing works
Maternal obesity and fetal metabolic programming: a fertile epigenetic soil
Heerwagen, M. J. R., Miller, M. R., Barbour, L. A., & Friedman, J. E. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00310.2010 · Cited by 520 · see citing works
Self-citationVerdile, G., Keane, K. N., Cruzat, V. F., Medic, S., Sabale, M., Rowles, J., Wijesekara, N., Martins, R. N., Fraser, P. E., & Newsholme, P. (2015) · Mediators of Inflammation · doi:10.1155/2015/105828 · Cited by 501 · see citing works
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 · see citing works
The Role of Placental Hormones in Mediating Maternal Adaptations to Support Pregnancy and Lactation
Napso, T., Yong, H. E. J., Lopez-Tello, J., & Sferruzzi-Perri, A. N. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01091 · Cited by 470 · see citing works
Draznin, B. (2006) · Diabetes · doi:10.2337/db06-0391 · Cited by 390 · see citing works
Self-citationKeane, K. N., Cruzat, V. F., Carlessi, R., de Bittencourt, P. I. H., & Newsholme, P. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/181643 · Cited by 392 · see citing works
Molecular mechanisms of insulin resistance in type 2 diabetes mellitus
Saini, V. (2010) · World Journal of Diabetes · doi:10.4239/wjd.v1.i3.68 · Cited by 292 · see citing works
Role of the GH/IGF-1 axis in lifespan and healthspan: Lessons from animal models
Berryman, D. E., Christiansen, J. S., Johannsson, G., Thorner, M. O., & Kopchick, J. J. (2008) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2008.05.005 · Cited by 288 · see citing works
Metabolic functions of glucocorticoid receptor in skeletal muscle
Kuo, T., Harris, C. A., & Wang, J.-C. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.03.003 · Cited by 240 · see citing works
Regulation of phosphoinositide 3-kinase expression in health and disease
Kok, K. B., Geering, B., & Vanhaesebroeck, B. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.01.003 · Cited by 231 · see citing works
Bandyopadhyay, G. K., Yu, J. G., Ofrecio, J., & Olefsky, J. M. (2005) · Diabetes · doi:10.2337/diabetes.54.8.2351 · Cited by 210 · see citing works
Magee, M., Permezel, M., Riley, C. B., Desoyé, G., & Lappas, M. (2009) · European Journal of Endocrinology · doi:10.1530/eje-09-0031 · Cited by 207 · see citing works
PIK3R1 Mutations Cause Syndromic Insulin Resistance with Lipoatrophy
Thauvin‐Robinet, C., Auclair, M., Duplomb, L., Caron, M., Avila, M., St‐Onge, J., Merrer, M. F. L., Luyer, B. L., Héron, D., Mathieu‐Dramard, M., et al. (2013) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2013.05.019 · Cited by 201 · see citing works
Sirt1 enhances skeletal muscle insulin sensitivity in mice during caloric restriction
Schenk, S., McCurdy, C. E., Philp, A., Chen, M. Z., Holliday, M. J., Bandyopadhyay, G. K., Osborn, O., Baar, K., & Olefsky, J. M. (2011) · Journal of Clinical Investigation · doi:10.1172/jci58554 · Cited by 197 · see citing works
Winnay, J. N., Boucher, J., Mori, M. A., Ueki, K., & Kahn, C. R. (2010) · Nature Medicine · doi:10.1038/nm.2121 · Cited by 191 · see citing works
Effects of growth hormone on glucose metabolism and insulin resistance in human
Kim, S.-H., & Park, M.-J. (2017) · Annals of Pediatric Endocrinology & Metabolism · doi:10.6065/apem.2017.22.3.145 · Cited by 181 · see citing works
Brachmann, S. M., Ueki, K., Engelman, J. A., Kahn, R., & Cantley, L. C. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.5.1596-1607.2005 · Cited by 177 · see citing works
The intricate role of growth hormone in metabolism
Vijayakumar, A., Yakar, S., & LeRoith, D. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00032 · Cited by 179 · see citing works
Luo, J., Field, S. J., Lee, J. Y., Engelman, J. A., & Cantley, L. C. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200503088 · Cited by 172 · see citing works
Dominici, F. P., Argentino, D. P., Muñoz, M. C., Miquet, J. G., Sotelo, A. I., & Turyn, D. (2005) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2005.07.001 · Cited by 168 · see citing works
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., & Thorner, M. O. (2007) · Diabetes · doi:10.2337/db06-0299 · Cited by 164 · see citing works
Self-citationThe Role of Placental Nutrient Sensing in Maternal-Fetal Resource Allocation1
Díaz, P., Powell, T. L., & Jansson, T. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.114.121798 · Cited by 158 · see citing works
Taniguchi, C. M., Tran, T. T., Kondo, T., Luo, J., Ueki, K., Cantley, L. C., & Kahn, C. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604628103 · Cited by 152 · see citing works
Kuo, T., Lew, M. J., Mayba, O., Harris, C. A., Speed, T. P., & Wang, J.-C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111334109 · Cited by 146 · see citing works
Barbour, L. A., Rahman, S. M., Gurevich, I., Leitner, J. W., Fischer, S. J., Roper, M. D., Knotts, T. A., Vo, Y., McCurdy, C. E., Yakar, S., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m506967200 · Cited by 143 · see citing works
Self-citationNair, S., Jayabalan, N., Guanzon, D., Palma, C., Scholz‐Romero, K., Elfeky, O. W. M., Zuñiga, F. A., Ormazábal, V., Diaz, E., Rice, G. E., et al. (2018) · Clinical Science · doi:10.1042/cs20180487 · Cited by 144 · see citing works
Pathophysiology of Gestational Diabetes Mellitus
Berberoglu, Z. (2019) · EMJ Diabetes · doi:10.33590/emjdiabet/10313616 · Cited by 129 · see citing works
Molecular pathways disrupted by gestational diabetes mellitus.
Nguyen-Ngo, C., Jayabalan, N., Salomon, C., & Lappas, M. (2019) · Journal of Molecular Endocrinology · doi:10.1530/jme-18-0274 · Cited by 103 · see citing works
Freemark, M. (2006) · Hormone Research in Paediatrics · doi:10.1159/000091505 · Cited by 118 · see citing works
Wright, S. C. E., Vasilevski, N., Serra, V., Rodon, J. A., & Eichhorn, P. J. A. (2021) · Cancers · doi:10.3390/cancers13071538 · Cited by 110 · see citing works
Wada, T., Hori, S., Sugiyama, M., Fujisawa, E., Nakano, T., Tsuneki, H., Nagira, K., Saito, S., & Sasaoka, T. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00649.2009 · Cited by 103 · see citing works
Stimulation of Human Trophoblast Invasion by Placental Growth Hormone
Lacroix, M.-C., Guibourdenche, J., Fournier, T., Laurendeau, I., Igout, A., Goffin, V., Pantel, J., Tsatsaris, V., & Evain‐Brion, D. (2005) · Endocrinology · doi:10.1210/en.2004-1550 · Cited by 102 · see citing works
The Role of PIK3R1 in Metabolic Function and Insulin Sensitivity
Tsay, A., & Wang, J.-C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612665 · Cited by 101 · see citing works
Reversal of Insulin Resistance Postpartum Is Linked to Enhanced Skeletal Muscle Insulin Signaling
Kirwan, J. P., Varastehpour, A., Jing, M. X., Presley, L. H., Shao, J., Friedman, J. E., & Catalano, P. M. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0749 · Cited by 96 · see citing works
Self-citationEffect of growth hormone on insulin signaling
Sharma, R., Kopchick, J. J., Puri, V., & Sharma, V. M. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111038 · Cited by 97 · see citing works
Mellor, P., Furber, L. A., Nyarko, J. N. K., & Anderson, D. H. (2011) · Biochemical Journal · doi:10.1042/bj20111164 · Cited by 90 · see citing works
PI3K signaling effects in hypothalamic neurons mediated by estrogen
Malyala, A., Zhang, C., Bryant, D. N., Kelly, M. J., & Rønnekleiv, O. K. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21584 · Cited by 87 · see citing works
Feng, H., Su, R., Song, Y., Wang, C., Lin, L., Ma, J., & Yang, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157185 · Cited by 86 · see citing works
James‐Allan, L. B., Rosario, F., Barner, K., Lai, A., Guanzon, D., McIntyre, D. H., Lappas, M., Powell, T. L., Salomón, C., & Jansson, T. (2020) · The FASEB Journal · doi:10.1096/fj.201902522rr · Cited by 82 · see citing works
Overlapped Metabolic and Therapeutic Links between Alzheimer and Diabetes
Ahmad, W. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8352-z · Cited by 80 · see citing works
Cornford, A. S., Barkan, A. L., & Horowitz, J. F. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1895 · Cited by 79 · see citing works
Ghrelin: a metabolic signal affecting the reproductive system
Lorenzi, T., Meli, R., Marzioni, D., Morroni, M., Baragli, A., Castellucci, M., Gualillo, O., & Muccioli, G. (2009) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2009.02.003 · Cited by 69 · see citing works
The Placental Role in Gestational Diabetes Mellitus: A Molecular Perspective
Calvo, M. C. C., Parra, H., Santeliz, R., Bautista, J., Luzardo, E., Villasmil, N., Martínez, M. S., Chacín, M., Cano, C., Checa-Ros, A., et al. (2024) · touchREVIEWS in Endocrinology · doi:10.17925/ee.2024.20.1.5 · Cited by 73 · see citing works
Aspects of placental growth hormone physiology
Fuglsang, J., & Ovesen, P. (2006) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2006.03.010 · Cited by 66 · see citing works
Beyond the metabolic role of ghrelin: A new player in the regulation of reproductive function
Muccioli, G., Lorenzi, T., Lorenzi, M., Ghé, C., Arnoletti, E., Raso, G. M., Castellucci, M., Gualillo, O., & Meli, R. (2011) · Peptides · doi:10.1016/j.peptides.2011.10.020 · Cited by 65 · see citing works
Arumugam, R., Horowitz, E., Lu, D., Collier, J. J., Ronnebaum, S. M., Fleenor, D., & Freemark, M. (2008) · Endocrinology · doi:10.1210/en.2008-0051 · Cited by 61 · see citing works
Sferruzzi-Perri, A. N., Lopez-Tello, J., Napso, T., & Yong, H. E. J. (2020) · Placenta · doi:10.1016/j.placenta.2020.01.015 · Cited by 58 · see citing works
Barbour, L. A. (2019) · Diabetes Care · doi:10.2337/dci18-0048 · Cited by 57 · see citing works
Self-citationEarly responses of insulin signaling to high-carbohydrate and high-fat overfeeding
Adochio, R., Leitner, J. W., Gray, K., Draznin, B., & Cornier, M. (2009) · Nutrition & Metabolism · doi:10.1186/1743-7075-6-37 · Cited by 56 · see citing works
Self-citationPlacental growth hormone is increased in the maternal and fetal serum of patients with preeclampsia
Mittal, P., Espinoza, J., Hassan, S. S., Kusanovic, J. P., Edwin, S. S., Nien, J. K., Gotsch, F., Than, N. G., Erez, O., Mazaki‐Tovi, S., et al. (2007) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050701463571 · Cited by 54 · see citing works
Regulation of p110δ PI 3-Kinase Gene Expression
Kok, K. B., Nock, G. E., Verrall, E. A. G., Mitchell, M., Hommes, D. W., Peppelenbosch, M. P., & Vanhaesebroeck, B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005145 · Cited by 50 · see citing works
Insulin resistance and diabetes caused by genetic or diet-induced KBTBD2 deficiency in mice
Zhang, Z., Turer, E. E., Li, X., Zhan, X., Choi, M., Tang, M., Press, A., Smith, S. R., Divoux, A., Moresco, E. M. Y., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1614467113 · Cited by 50 · see citing works
Browne, I. M., & Okines, A. F. C. (2024) · Cancers · doi:10.3390/cancers16122259 · Cited by 50 · see citing works
Raison d’être of insulin resistance: the adjustable threshold hypothesis
Wang, G. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2014.0892 · Cited by 47 · see citing works
Jones, R. L., Cederberg, H., Wheeler, S., Poston, L., Hutchinson, C., Seed, P. T., Oliver, R. L., & Baker, P. N. (2009) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2009.02371.x · Cited by 45 · see citing works
Huo, J. S., McEachin, R. C., Cui, T. X., Duggal, N. K., Hai, T., States, D. J., & Schwartz, J. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508492200 · Cited by 44 · see citing works
Does the Physiological Acromegaly of Pregnancy Benefit the Fetus?
Verhaeghe, J. (2008) · Gynecologic and Obstetric Investigation · doi:10.1159/000147167 · Cited by 43 · see citing works
Insulin receptor isoforms: an integrated view focused on gestational diabetes mellitus
Westermeier, F., Sáez, T., Arroyo, P., Toledo, F., Gutiérrez, J., Sanhueza, C., Pardo, F., Leiva, A., & Sobrevía, L. (2015) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2729 · Cited by 42 · see citing works
Effects of growth hormone in the central nervous system
Wasinski, F., Frazão, R., & Donato, J. (2019) · Archives of Endocrinology and Metabolism · doi:10.20945/2359-3997000000184 · Cited by 42 · see citing works
Chapter 6 Crosstalk Between Growth Hormone and Insulin Signaling
Xu, J., & Messina, J. L. (2009) · Vitamins and hormones · doi:10.1016/s0083-6729(08)00606-7 · Cited by 40 · see citing works
Sadri, H., Bruckmaier, R. M., Rahmani, H. R., Ghorbani, G. R., Morel, I., & van Dorland, H. A. (2010) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/j.1439-0396.2010.01005.x · Cited by 40 · see citing works
Trollmann, R., Klingmüller, K., Schild, R. L., Rascher, W., & Dötsch, J. (2007) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.04.008 · Cited by 38 · see citing works
Cornier, M.-A., Bessesen, D. H., Gurevich, I., Leitner, J. W., & Draznin, B. (2006) · Diabetologia · doi:10.1007/s00125-006-0148-0 · Cited by 35 · see citing works
Self-citationNair, S., & Salomón, C. (2020) · Placenta · doi:10.1016/j.placenta.2020.06.011 · Cited by 37 · see citing works
Igf2 deletion alters mouse placenta endocrine capacity in a sexually dimorphic manner
Aykroyd, B. R. L., Tunster, S. J., & Sferruzzi-Perri, A. N. (2020) · Journal of Endocrinology · doi:10.1530/joe-20-0128 · Cited by 34 · see citing works
Zeck, W., Widberg, C., Maylin, E. R., Desoyé, G., Lang, U., McIntyre, D. H., Prins, J. B., & Russell, A. W. (2008) · Pediatric Research · doi:10.1203/01.pdr.0000304935.19183.07 · Cited by 34 · see citing works
Argentino, D. P., Dominici, F. P., Muñoz, M. C., Al-Regaiey, K., Bartke, A., & Turyn, D. (2004) · Experimental Gerontology · doi:10.1016/j.exger.2004.09.005 · Cited by 33 · see citing works
Gene Expression Profiling of Type 2 Diabetes Mellitus by Bioinformatics Analysis
Zhu, H., Zhu, X., Liu, Y., Jiang, F., Chen, M., Cheng, L., & Cheng, X. (2020) · Computational and Mathematical Methods in Medicine · doi:10.1155/2020/9602016 · Cited by 33 · see citing works
Biochemical and Molecular Biomarkers: Unraveling Their Role in Gestational Diabetes Mellitus
Karami, M., Mousavi, S. H., Rafiee, M., Heidari, R., & Shahrokhi, S. Z. (2023) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-023-00980-8 · Cited by 33 · see citing works
Maternal and Fetal Placental Growth Hormone and IGF Axis in Type 1 Diabetic Pregnancy
Higgins, M., Russell, N. E., Crossey, P. A., Nyhan, K. C., Brazil, D. P., & McAuliffe, F. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029164 · Cited by 30 · see citing works
Gavete, M. L., Martín, M. Á., Álvarez, C., & Escrivá, F. (2005) · Endocrinology · doi:10.1210/en.2004-1658 · Cited by 30 · see citing works
Batista, M. R., Smith, M. S., Snead, W. L., Connolly, C. C., Lacy, D. B., & Moore, M. C. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00311.2005 · Cited by 30 · see citing works
Nair, S., Ormazábal, V., Lappas, M., McIntyre, D. H., & Salomón, C. (2020) · American Journal of Reproductive Immunology · doi:10.1111/aji.13361 · Cited by 29 · see citing works
Sadagurski, M., Weingarten, G., Rhodes, C. J., White, M. F., & Wertheimer, E. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m410227200 · Cited by 29 · see citing works
Early signal protein expression profiles in basophils: a population study
Ishmael, S. S., & MacGlashan, D. W. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.1208724 · Cited by 29 · see citing works
Kobayashi, T., Hayashi, Y., Taguchi, K., Matsumoto, T., & Kamata, K. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01349.2005 · Cited by 29 · see citing works
Karadoğan, A. H., Arıkoğlu, H., Göktürk, F., İşçioğlu, F., & İpekçi, S. H. (2018) · Advances in Clinical and Experimental Medicine · doi:10.17219/acem/68985 · Cited by 27 · see citing works
Peripartum maternal and foetal ghrelin, growth hormones, IGFs and insulin interrelations
Fuglsang, J., Sandager, P., Møller, N., Fisker, S., Frystyk, J., & Ovesen, P. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02498.x · Cited by 26 · see citing works
Zhao, L., Hao, L., Yang, X., Ying, C., Dong, Y., & Sun, X. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114508094646 · Cited by 26 · see citing works
Lizárraga, D., & Garcı́a-Gasca, A. (2021) · Epigenomes · doi:10.3390/epigenomes5020013 · Cited by 27 · see citing works
Pathophysiology of Gestational Diabetes Mellitus: The Past, the Present and the Future
Chyad, M., & Shalayel, M. H. F. (2011) · InTech eBooks · doi:10.5772/24315 · Cited by 24 · see citing works
Liao, S., Vickers, M. H., Stanley, J. L., Ponnampalam, A. P., Baker, P. N., & Perry, J. K. (2015) · Endocrinology · doi:10.1210/en.2015-1718 · Cited by 24 · see citing works
McIntyre, D. H. (2018) · Diabetes Care · doi:10.2337/dci17-0056 · Cited by 24 · see citing works
Melnik, B. C. (2009) · Medical Hypotheses · doi:10.1016/j.mehy.2009.04.047 · Cited by 23 · see citing works
James‐Allan, L. B., Rosario, F., Madi, L., Barner, K., Nair, S., Lai, A., Carrión, F., Powell, T. L., Salomón, C., & Jansson, T. (2022) · Clinical Science · doi:10.1042/cs20220484 · Cited by 21 · see citing works
O-GlcNAc transferase contributes to sex-specific placental deregulation in gestational diabetes
Cui, Y., Cruz, M., Palatnik, A., & Stichelen, S. O.-V. (2022) · Placenta · doi:10.1016/j.placenta.2022.11.006 · Cited by 21 · see citing works
Insulinoma associated with pregnancy
Díaz, A. G., Herrera, J., López, M., Puchulu, F. M., Ferraina, P. A., & Bruno, O. D. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.06.092 · Cited by 21 · see citing works
Adochio, R., Leitner, J. W., Hedlund, R., & Draznin, B. (2008) · Endocrinology · doi:10.1210/en.2008-0437 · Cited by 21 · see citing works
Self-citationPlacental Endocrine Function and Hormone Action
Albrecht, E. D., & Pepe, G. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00040-5 · Cited by 20 · see citing works
Magnetic Bead-Based Serum Peptidome Profiling in Patients with Gestational Diabetes Mellitus
Ai, T., Chen, F., Zhou, S., Zhang, J., Zheng, H., Zhou, Y., Hu, W. M., Liu, X., Li, L., & Lin, J. (2015) · BioMed Research International · doi:10.1155/2015/586309 · Cited by 19 · see citing works
Vickers, M. H., Gilmour, S., Gertler, A., Breier, B. H., Tunny, K. A., Waters, M. J., & Gluckman, P. D. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00221.2009 · Cited by 19 · see citing works
Advances in extracellular vesicles as mediators of cell-to-cell communication in pregnancy
Nair, S., Razo-Azamar, M., Jayabalan, N., Dalgaard, L. T., Palacios‐González, B., Sørensen, A., Kampmann, U., Handberg, A., Carrión, F., & Salomón, C. (2023) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2023.12.004 · Cited by 20 · see citing works
Genetic and Epigenetic Factors in Gestational Diabetes Mellitus Pathology
Ustianowski, Ł., Udzik, J., Szostak, J., Gorący, A., Ustianowska, K., & Pawlik, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242316619 · Cited by 17 · see citing works
- Authors
- Barbour, L. A., Shao, J., Qiao, L., Leitner, W., Anderson, M., Friedman, J. E., & Draznin, B.
- Affiliations
- Department of Medicine (L.A.B., B.D.), Denver, Colorado 80262
- Department of Pediatrics (J.S., L.Q., M.A., J.E.F.), Denver, Colorado 80262
- University of Colorado Health (US)
- Corresponding author
- Barbour, Linda A.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2004-03-01
- Volume
- 145
- Issue
- 3
- Pages
- 1144-1150
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W2111953703
- Cited by
- 208
- References
- 27
- Citations by year
- 2025: 4 · 2024: 4 · 2023: 24 · 2022: 6 · 2021: 10 · 2020: 12 · 2019: 12 · 2018: 8 · 2017: 6 · 2016: 6 · 2015: 11 · 2014: 6 · 2013: 6 · 2012: 13
- FWCI
- 5.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01dk062155-04)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-62155)
- National Center for Research Resources (K23RR017496, 1K23-RR-017496-01)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Keywords
- placental growth hormone, insulin resistance, skeletal muscle, phosphatidylinositol 3-kinase, IRS-1, GLUT4 translocation, insulin receptor, p110 catalytic subunit, transgenic mice, pregnancy, dominant negative regulation, insulin signaling
- MeSH terms
- Placenta Growth Factor, Animals, Cell Membrane, Humans, Insulin Resistance, Mice, Transgenic, Monosaccharide Transport Proteins, Muscle Proteins, Phosphoproteins, Phosphorylation, Pregnancy Proteins, Receptor, Insulin, Signal Transduction, Protein Structure, Tertiary, Muscle, Skeletal, Phosphatidylinositol 3-Kinases, Glucose Transporter Type 4, Mice, Insulin Receptor Substrate Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
